Skip to main content
Log in

Growth Responses, Metal Accumulation and Phytoremoval Capability in Amaranthus Plants Exposed to Nickel Under Hydroponics

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

Abstract

The characterisation of plant responses to metal exposure represents a basic step to select a plant species for phytoremediation. In the present work, 3-week-old Amaranthus paniculatus L. plants were subjected to nickel chloride concentrations of 0 (control), 25, 50, 100 and 150 μM in hydroponic solution for 1 week to evaluate morphophysiological responses, such as biomass production and partitioning, nickel accumulation in plants and nickel removal ability from the polluted solutions. The results showed a progressive decrease in plant organ dry mass with the enhancement of nickel (Ni) concentration in the solution, suggesting a good metal tolerance at 25 μM Ni and a marked sensitivity at 150 μM Ni. The modification of biomass partitioning was particularly appreciated in leaves, analysing the organ mass ratio, the total leaf area and the specific leaf area. Amaranthus plants accumulated a significant amount of Ni in roots exposed to the highest Ni concentrations, while lower metal contents were observed in the aerial organs. The Ni uptake ratio was progressively reduced in plants exposed to increased Ni concentrations. The metal translocation from root to shoots, appreciated by the Ni translocation index, showed a far lower value in Ni-exposed plants than in controls. Moreover, by measuring the daily Ni content of the solutions, a lower Ni removal ability was found in Amaranthus plants at increasing Ni concentrations. Remarkably, plants exposed to 25 μM Ni succeeded in removing almost 60 % of the initial Ni content of the solution showing no stress symptoms. The potential of A. paniculatus for phytoremediation was discussed.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Assunção, A. G. L., Bookum, W. M., Nelissen, H. J. M., Vooijs, R., Schat, H., & Ernst, W. H. O. (2003). Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytologist, 159, 411–419.

    Article  Google Scholar 

  • Audet, P., & Charest, C. (2008). Allocation plasticity and plant–metal partitioning: meta-analytical perspectives in phytoremediation. Environmental Pollution, 156, 290–296.

    Article  CAS  Google Scholar 

  • Bai, C., Reilly, C. C., & Wood, B. W. (2006). Nickel deficiency disrupts metabolism of ureides, amino acids, and organic acids of young pecan foliage. Plant Physiology, 140, 433–443.

    Article  CAS  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 

  • Baker, A. J. M., & Brooks, R. R. (1989). Terrestrial higher plants which accumulate metallic elements: a review of their distribution, ecology and phytochemistry. Biorecovery, 1, 81–126.

    CAS  Google Scholar 

  • Chen, C., Huang, D., & Liu, J. (2009). Functions and toxicity of nickel in plants: recent advances and future prospects. Clean, 37, 304–313.

    CAS  Google Scholar 

  • Di Baccio, D., Minnocci, A., & Sebastiani, L. (2010). Leaf structural modifications s in Populus × euramericana subjected to Zn excess. Biologia Plantarum, 54, 502–508.

    Article  CAS  Google Scholar 

  • Dos Santos Utmazian, M. N., Wieshammer, G., Vega, R., & Wenzel, W. W. (2007). Hydroponic screening for metal resistance and accumulation of cadmium and zinc in twenty clones of willows and poplars. Environmental Pollution, 148, 155–165.

    Article  Google Scholar 

  • Farkas, A., Erratico, C., & Viganò, L. (2007). Assessment of the environmental significance of heavy metal pollution in surficial sediments of the River Po. Chemosphere, 68, 761–768.

    Article  CAS  Google Scholar 

  • Fatta-Kassinos, D., Kalavrouziotis, I. K., Koukoulakis, P. H., & Vasquez, M. I. (2011). The risk associated with wastewater reuse and xenobiotics in the agroecological environment. Science of the Total Environment, 409, 3555–3563.

    Article  CAS  Google Scholar 

  • Fernandez, J., Zacchini, M., & Fleck, I. (2012). Photosynthetic and growth responses of Populus clones Eridano and I-214 submitted to elevated Zn concentrations. Journal of Geochemical Exploration. doi:10.1016/j.gexplo.2012.01.010.

  • Gabbrielli, R., Mattioni, C., & Vergnano, O. (1991). Accumulation mechanisms and heavy metal tolerance of a nickel hyperaccumulator. Journal of Plant Nutrition, 14, 1067–1080.

    Article  CAS  Google Scholar 

  • Galardi, F., Corrales, I., Mengoni, A., Pucci, S., Barletti, L., Barzanti, R., et al. (2007). Intra-specific differences in nickel tolerance and accumulation in the Ni-hyperaccumulator Alyssum bertolonii. Environmental and Experimental Botany, 60, 377–384.

    Article  CAS  Google Scholar 

  • Hassan, Z., & Aarts, M. G. M. (2011). Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environmental and Experimental Botany, 72, 53–63.

    Article  CAS  Google Scholar 

  • Iori, V., Pietrini, F., Massacci, A., & Zacchini, M. (2012). Induction of metal binding compounds and antioxidative defence in callus cultures of two black poplar (P. nigra) clones with different tolerance to cadmium. Plant Cell Tissue and Organ Culture, 108, 17–26.

    Article  CAS  Google Scholar 

  • Kotyza, J., Soudek, P., Kafka, Z., & Vanĕk, T. (2010). Phytoremediation of pharmaceuticals—preliminary study. International Journal of Phytoremediation, 12, 306–316.

    Article  CAS  Google Scholar 

  • Kováčik, J., Klejdus, B., Hedbavny, J., & Bačkor, M. (2009). Nickel uptake and its effect on some nutrient levels, amino acid contents and oxidative status in Matricaria chamomilla plants. Water, Air, and Soil Pollution, 202, 199–209.

    Article  Google Scholar 

  • Kramer, U. (2010). Metal hyperaccumulation in plants. Annual Review of Plant Biology, 61, 517–534.

    Article  Google Scholar 

  • Kramer, U., Smith, R. D., Wenzel, W. W., Raskin, I., & Salt, D. E. (1997). The role of metal transport and tolerance in nickel hyperaccumulation by Thlaspi goesingense Hálácsy. Plant Physiology, 115, 1641–1650.

    CAS  Google Scholar 

  • Küpper, H., & Kroneck, P. M. H. (2007). Nickel in the environment and its role in the metabolism of plants and cyanobacteria. In: Sigel, A., Sigel, H., Sigel, R. K. O. (Eds), Metal ions in life sciences, vol 2. Hoboken, NJ, USA: Wiley, pp 31–62.

  • Leblebici, Z., & Aksoy, A. (2011). Growth and lead accumulation capacity of Lemna minor and Spirodela polyrhiza (Lemnaceae): interactions with nutrient enrichment. Water, Air, and Soil Pollution, 214, 345–356.

    Article  Google Scholar 

  • Li, N. Y., Li, Z. A., Zhuang, P., Zou, B., & McBride, M. (2009). Cadmium uptake from soil by maize with intercrops. Water, Air, and Soil Pollution, 199, 45–56.

    Article  CAS  Google Scholar 

  • Licht, L. A., & Isebrands, J. G. (2005). Linking phytoremediated pollutant removal to biomass economic opportunities. Biomass and Bioenergy, 28, 203–218.

    Article  CAS  Google Scholar 

  • Llamas, A., Ullrich, C. L., & Sanz, A. (2008). Ni2+ toxicity in rice: effect on membrane functionality and plant water content. Plant Physiology and Biochemistry, 46, 905–910.

    Article  CAS  Google Scholar 

  • Long, S. P. (1999). Environmental responses. In R. F. Sage & R. K. Monson (Eds.), C4 plant biology (pp. 215–249). San Diego: Academic.

    Chapter  Google Scholar 

  • Madzhugina, Y. G., Kuznetsov, V. V., & Shevyakova, N. I. (2008). Plants inhabiting polygons for megapolis waste as promising species for phytoremediation. Russian Journal of Plant Physiology, 55, 410–419.

    Article  CAS  Google Scholar 

  • Marchiol, L., Sacco, P., Assolati, S., & Zerbi, G. (2004). Reclamation of polluted soil: phytoremediation potential of crop-related Brassica species. Water, Air, and Soil Pollution, 158, 345–356.

    Article  CAS  Google Scholar 

  • Marmiroli, M., Pietrini, F., Maestri, E., Zacchini, M., Marmiroli, N., & Massacci, A. (2011). Growth, physiological and molecular traits in Salicaceae trees investigated for phytoremediation of heavy metals and organics. Tree Physiology, 31, 1319–1334.

    Article  CAS  Google Scholar 

  • Mellem, J. J., Baijnath, H., & Odhav, B. (2009). Translocation and accumulation of Cr, Hg, As, Pb, Cu and Ni by Amaranthus dubius (Amaranthaceae) from contaminated sites. Journal of Environmental Science and Health, 44, 568–575.

    Article  CAS  Google Scholar 

  • Nieminen, T. M., Ukonmaanaho, L., Rausch, N., & Shotyk, W. (2007). Biogeochemistry of nickel and its release into the environment. In: Sigel, A., Sigel, H., Sigel, R. K. O. (Eds) Metal ions in life sciences, vol. 2. Hoboken, NJ, USA Wiley, pp 1–30.

  • Padmavathiamma, P. K., & Li, L. Y. (2007). Phytoremediation technology: hyper-accumulation metals in plants. Water, Air, and Soil Pollution, 184, 105–126.

    Article  CAS  Google Scholar 

  • Pereira, M. C., Pereira, M. L., & Sousa, J. P. (2002). Evaluation of nickel toxicity on liver, spleen, and kidney of mice after administration of high-dose metal ion. Journal of Biomedical Materials Research, 40, 40–47.

    Article  Google Scholar 

  • Pietrini, F., Zacchini, M., Pietrosanti, L., Iori, V., Bianconi, D., & Massacci, A. (2010). Screening of poplar clones for cadmium phytoremediation using photosynthesis, biomass and cadmium content analyses. International Journal of Phytoremediation, 12, 105–120.

    Article  CAS  Google Scholar 

  • Pietrini, F., Zacchini, M., Iori, V., Pietrosanti, L., Ferretti, M., & Massacci, A. (2010). Spatial distribution of cadmium in leaves and its impact on photosynthesis: examples of different strategies in willow and poplar clones. Plant Biology, 12, 355–363.

    Article  CAS  Google Scholar 

  • Prasad, M. N. V. (2003). Phytoremediation of metal-polluted ecosystems: hype for commercialization. Russian Journal of Plant Physiology, 50, 764–780.

    Article  Google Scholar 

  • Prasad, M. N. V., & Freitas, H. M. O. (2003). Metal hyperaccumulation in plants—biodiversity prospecting for phytoremediation technology. Electronic Journal of Biotechnology, 6, 285–321.

    Article  Google Scholar 

  • Pyle, G. G., Swanson, S. M., & Lehmkuhl, D. M. (2002). The influence of water hardness, pH, and suspended solids on nickel toxicity to larval fathead minnows (Pimephales promelas). Water, Air, and Soil Pollution, 133, 215–226.

    Article  CAS  Google Scholar 

  • Robinson, B. H., Chiarucci, A., Brooks, R. R., Petit, D., Kirkman, J. H., Gregg, P. E. H., et al. (1997). The nickel hyperaccumulator plant Alyssum bertolonii as a potential agent for phytoremediation and phytomining of nickel. Journal of Geochemical Exploration, 59, 75–86.

    Article  CAS  Google Scholar 

  • Robinson, B. H., Lombi, E., Zhao, F. J., & McGrath, S. P. (2003). Uptake and distribution of nickel and other metals in the hyperaccumulator Berkheya coddii. New Phytologist, 158, 279–285.

    Article  CAS  Google Scholar 

  • Sage, R. F., & Pearcy, R. W. (1987). The nitrogen use efficiency of C3 and C4 plants II. Leaf nitrogen effects on the gas exchange characteristics of Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiology, 84, 959–963.

    Article  CAS  Google Scholar 

  • Sanz, A., Llamas, A., & Ullrich, C. I. (2009). Distinctive phytotoxic effects of Cd and Ni on membrane functionality. Plant Signaling & Behavior, 4, 980–982.

    Article  CAS  Google Scholar 

  • Schwitzguébel, J. P., Kumpiene, J., Comino, E., & Vanek, T. (2009). From green to clean: a promising and sustainable approach towards environmental remediation and human health for the 21st century. Agrochimica, 53, 1–29.

    Google Scholar 

  • Sebastiani, L., Scebba, F., & Tognetti, R. (2004). Heavy metal accumulation and growth responses in poplar clones Eridano (Populus deltoides × maximowiczii) and I-214 (P. × euramericana) exposed to industrial waste. Environmental and Experimental Botany, 52, 79–88.

    Article  CAS  Google Scholar 

  • Seregin, I. V., & Kozhevnikova, A. D. (2006). Physiological role of nickel and its toxic effects on higher plants. Russian Journal of Plant Physiology, 53, 285–308.

    Article  Google Scholar 

  • Shevyakova, N. I., Cheremisina, A., & Kuznetsov, V. V. (2011). Phytoremediation potential of Amaranthus hybrids: antagonism between nickel and iron and chelating role of polyamines. Russian Journal of Plant Physiology, 58, 634–642.

    Article  CAS  Google Scholar 

  • Singer, A. C., Bell, T., Heywood, C. A., Smith, J. A. C., & Thompson, I. P. (2007). Phytoremediation of mixed-contaminated soil using the hyperaccumulator plant Alyssum lesbiacum: evidence of histidine as a measure of phytoextractable nickel. Environmental Pollution, 147, 74–82.

    Article  CAS  Google Scholar 

  • Vassilev, A., Berova, M., & Zlatev, Z. (1998). Influence of Cd2+ on growth, chlorophyll content, and water relations in young barley plants. Biologia Plantarum, 41, 601–606.

    Article  CAS  Google Scholar 

  • Wenzel, W. W., Bunkowski, M., Pushenreiter, M., & Horak, O. (2003). Rhizosphere characteristics of indigenously growing nickel hyperaccumulator and excluder plants on serpentine soil. Environmental Pollution, 123, 131–138.

    Article  CAS  Google Scholar 

  • Zacchini, M., Pietrini, F., Scarascia Mugnozza, G., Iori, V., Pietrosanti, L., & Massacci, A. (2009). Metal tolerance, accumulation and translocation in poplar and willow clones treated with cadmium in hydroponics. Water, Air, and Soil Pollution, 197, 23–34.

    Article  CAS  Google Scholar 

  • Zhang, X., Zhang, S., Xu, X., Li, T., Gong, G., Jia, Y., et al. (2010). Tolerance and accumulation characteristics of cadmium in Amaranthus hybridus L. Journal of Hazardous Materials, 180, 303–308.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was realised within the joint project between National Research Council of Italy and Russian Academy of Sciences “Mechanisms of plant adaptation to stress action of heavy metals: possible implications for the phytoremediation technology”. Authors wish to thank Mr. Ermenegildo Magnani for his expert technical assistance in metal content analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Massimo Zacchini.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Iori, V., Pietrini, F., Cheremisina, A. et al. Growth Responses, Metal Accumulation and Phytoremoval Capability in Amaranthus Plants Exposed to Nickel Under Hydroponics. Water Air Soil Pollut 224, 1450 (2013). https://doi.org/10.1007/s11270-013-1450-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-013-1450-3

Keywords

Navigation