Skip to main content
SpringerLink
Log in

Variation in Copper Accumulation at the Tissue Level of Five Hybrid Poplars Subjected to Copper Stress

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

Abstract

Heavy metal contamination causes significant environmental problems around the world and poses a threat to human health. Poplar hybrids present features for potential uses in phytoremediation systems in areas with heavy metal contamination. The purpose of this study was to assess the copper (Cu) accumulation level in five poplar inter-species hybrids [(Populus trichocarpa × Populus deltoides) × P. deltoides; P. deltoides × Populus nigra; P. trichocarpa × Populus maximowiczii; P. trichocarpa × P. nigra; and (P. trichocarpa × P. deltoides) × (P. trichocarpa × P. deltoides)] grown in a hydroponic system. The treatments entailed the application of low and high doses of Cu of 8.0 and 16.0 μM, respectively. Cu accumulation was observed in roots, stems, and leaves, which was determined using flame atomic absorption spectroscopy, prior acid digestion of each sample. The methodology was validated according to certified reference material (Cypress BIMEP 432). Significant differences in Cu accumulation were found among genotypes for both roots and leaves, but not for stems. In roots, the genotype P. deltoides × P. nigra had a Cu accumulation level of 169.8% higher than the average accumulation found in the other genotypes. The (P. trichocarpa × P. deltoides) × P. deltoides hybrid showed the least Cu accumulation in leaves. The results of this study can potentially be used for proper crossovers and hybrids selection within the genus Populus for phytoremediation of Cu contaminated land.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

References

  • Allen, S.E., Grimshaw, H.M., & Rowland, A.P. (1986). Chemical analysis. Methods in plant ecology. (Eds PD Moore, SB Chapman). p. 285–344.

  • Anjum, N. A., Adam, V., Kizek, R., Duarte, A. C., Pereira, E., Iqbal, M., Lukatkin, A. S., & Ahmad, I. (2015). Nanoscale copper in the soil–plant system–toxicity and underlying potential mechanisms. Environmental Research, 138, 306–325.

    Article  CAS  Google Scholar 

  • Borghi, M., Tognetti, R., Monteforti, G., & Sebastiani, L. (2007). Responses of Populus× euramericana (P. deltoides × P. nigra) clone Adda to increasing copper concentrations. Environmental and Experimental Botany, 61(1), 66–73.

    Article  CAS  Google Scholar 

  • Borghi, M., Tognetti, R., Monteforti, G., & Sebastiani, L. (2008). Responses of two poplar species (Populus alba and Populus x canadensis) to high copper concentrations. Environmental and Experimental Botany, 62, 290–299.

    Article  CAS  Google Scholar 

  • Di Baccio, D., Tognetti, R., Sebastiani, L., & Vitagliano, C. (2003). Responses of Populus deltoides× Populus nigra (Populus× euramericana) clone I-214 to high zinc concentrations. The New Phytologist, 159(2), 443–452.

    Article  CAS  Google Scholar 

  • Evangelou, M. W., Ebel, M., & Schaeffer, A. (2007). Chelate assisted phytoextraction of heavy metals from soil. Effect, mechanism, toxicity, and fate of chelating agents. Chemosphere, 68(6), 989–1003.

    Article  CAS  Google Scholar 

  • Ginocchio, R., Toro, I., Schnepf, D., & Macnair, M. R. (2002). Copper tolerance testing in populations of Mimulus luteus var. variegatus exposed and non-exposed to copper mine pollution. Geochem-Explor Env A, 2(2), 151–156.

    Article  CAS  Google Scholar 

  • Ginocchio, R., Carvallo, G., Toro, I., Bustamante, E., Silva, Y., & Sepúlveda, N. (2004). Micro-spatial variation of soil metal pollution and plant recruitment near a copper smelter in Central Chile. Environmental Pollution, 127, 343–352.

    Article  CAS  Google Scholar 

  • Gomes, M., Marques, T., Carneiro, M., & Soares, A. (2012). Anatomical characteristics and nutrient uptake and distribution associated with the Cd-phytoremediation capacity of Eucalyptus camaldulenses Dehnh. Journal of Soil Science and Plant Nutrition, 12(3), 481–495.

    Google Scholar 

  • Guerra, F., Duplessis, S., Kohler, A., Martin, F., Tapia, J., Lebed, P., Zamudio, F., & González, E. (2009). Gene expression analysis of Populus deltoides roots subjected to copper stress. Environmental and Experimental Botany, 67(2), 335–344.

    Article  CAS  Google Scholar 

  • Guerra, F., Pérez, R., Gainza, F., & Zamudio, F. (2010). Phytoremediation of heavy metals using poplars (Populus spp.): a glimpse of the plant responses to copper, cadmium and zinc stress. In I. Golubev (Ed.), Handbook of phytoremediation (pp. 387–414). NY: Nova Science Publishers.

    Google Scholar 

  • Hassan, Z., & Aarts, M. G. (2011). Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environmental and Experimental Botany, 72(1), 53–63.

    Article  CAS  Google Scholar 

  • Houda, Z., Bejaoui, Z., Albouchi, A., Gupta, D. K., & Corpas, F. J. (2016). Comparative study of plant growth of two poplar tree species irrigated with treated wastewater, with particular reference to accumulation of heavy metals (Cd, Pb, As, and Ni). Environmental Monitoring and Assessment, 188(2), 1–10.

    Article  CAS  Google Scholar 

  • Karla, Y. P. (1998). Handbook of reference methods for plant analysis. USA: Soil and Plant Analysis Council, Inc., CRC Press 300 p.

    Google Scholar 

  • Kopponen, P., Utriainen, M., Lukkari, K., Suntioinen, S., Kärenlampi, L., & Kärenlampi, S. (2001). Clonal differences in copper and zinc tolerance of birch in metal-supplemented soils. Environmental Pollution, 112(1), 89–97.

    Article  CAS  Google Scholar 

  • Kuzovkina, Y. A., Knee, M., & Quigley, M. F. (2004). Cadmium and copper uptake and translocation in five willow (Salix L.) species. International Journal of Phytoremediation, 6(3), 269–287.

    Article  CAS  Google Scholar 

  • Laureysens, I., Blust, R., De Temmerman, L., Lemmens, C., & Ceulemans, R. (2004). Clonal variation in heavy metal accumulation and biomass production in a poplar coppice culture: I. Seasonal variation in leaf, wood and bark concentrations. Environmental Pollution, 131(3), 485–494.

    Article  CAS  Google Scholar 

  • Lebrun, M. (2001). Phytoremediation of toxic metals. In I. Raskin & B. Ensley (Eds.), Using plants to clean up the environment. New York: John Wiley & Sons, Inc. 2000.

    Google Scholar 

  • Lu, L. L., Tian, S. K., Yang, X. E., Peng, H. Y., & Li, T. Q. (2013). Improved cadmium uptake and accumulation in the hyperaccumulator Sedum alfredii: the impact of citric acid and tartaric acid. Journal of Zhejiang University. Science. B, 14(2), 106–114.

    Article  CAS  Google Scholar 

  • McLaughlin, M. J., Smolders, E., Degryse, F., & Rietra, R. (2011). Uptake of metals from soil into vegetables. In dealing with contaminated sites (pp. 325–367). Netherlands: Springer.

    Book  Google Scholar 

  • Migeon, A., Richaud, P., Guinet, F., Chalot, M., & Blaudez, D. (2009). Metal accumulation by woody species on contaminated sites in the north of France. Water Air Soil Poll, 204(1–4), 89–101.

    Article  CAS  Google Scholar 

  • Parelho, C., Rodrigues, A. S., Cruz, J. V., & Garcia, P. (2014). Linking trace metals and agricultural land use in volcanic soils—a multivariate approach. Science of the Total Environment, 496, 241–247.

    Article  CAS  Google Scholar 

  • Paschke, M. W., Perry, L. G., & Redente, E. F. (2006). Zinc toxicity thresholds for reclamation forb species. Water Air Soil Poll, 170(1–4), 317–330.

    Article  CAS  Google Scholar 

  • Peng, H. Y., Yang, X. E., & Tian, S. K. (2005). Accumulation and ultrastructural distribution of copper in Elsholtzia splendens. Journal of Zhejiang University. Science. B, 6(5), 311–318.

    Article  Google Scholar 

  • Pietrini, F., Zacchini, M., Iori, V., Pietrosanti, L., 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 

  • Pizarro, R., Flores, J. P., Tapia, J., Valdés-Pineda, R., González, D., Morales, C., Sangüesa, C., Balocchi, F., & León, L. (2016). Forest species in the recovery of soils contaminated with copper due to mining activities. Rev Chapingo. Ser Cie, 22(1), 29–43.

    Google Scholar 

  • Pollard, A. J., Powell, K. D., Harper, F. A., Andrew, J., & Smith, C. (2002). The genetic basis of metal hyperaccumulation in plants. Critical Reviews in Plant Sciences, 21, 539–566.

    Article  CAS  Google Scholar 

  • Pulford, I. D., & Watson, C. (2003). Phytoremediation of heavy metal-contaminated land by trees—a review. Environment International, 29(4), 529–540.

    Article  CAS  Google Scholar 

  • Punshon, T., Dickinson, N. M., & Lepp, N. W. (1996). The potential of Salix clones for bioremediating metal polluted soil. In heavy metals and trees. Proceedings of a Discussion Meeting, Glasgow (pp. 93–104). Edinburgh: Institute of Chartered Foresters.

    Google Scholar 

  • Purdy, J., & Smart, L. (2008). Hydroponic screening of shrub willow (Salix spp.) for arsenic tolerance and uptake. International Journal of Phytoremediation, 10(6), 515–528.

    Article  CAS  Google Scholar 

  • Robinson, B. H., Green, S. R., Chancerel, B., Mills, T. M., & Clothier, B. E. (2007). Poplar for the phytomanagement of boron contaminated sites. Environmental Pollution, 150(2), 225–233.

    Article  CAS  Google Scholar 

  • SDSG—Sustainable Development Strategies Group. (2012). Current issues in the Chilean mining sector. http://www.sdsg.org/wp-content/uploads/2010/02/10-10-08-CHILE-REPORT.pdf. Accessed 04 April 2017.

  • 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(1), 79–88.

    Article  CAS  Google Scholar 

  • Surat, W., Kruatrachue, M., Pokethitiyook, P., Tanhan, P., & Samranwanich, T. (2008). Potential of Sonchus arvensis for the phytoremediation of lead-contaminated soil. International Journal of Phytoremediation, 10(4), 325–342.

    Article  CAS  Google Scholar 

  • Sytar, O., Kumar, A., Latowski, D., Kuczynska, P., Strzałka, K., & Prasad, M. N. V. (2013). Heavy metal induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiologiae Plantarum, 35(4), 985–999.

    Article  CAS  Google Scholar 

  • Tanhan, P., Kruatrachue, M., Pokethitiyook, P., & Chaiyarat, R. (2007). Uptake and accumulation of cadmium, lead and zinc by Siam weed [Chromolaena odorata (L.) King & Robinson]. Chemosphere, 68(2), 323–329.

    Article  CAS  Google Scholar 

  • Tapia, J., Vargas-Chacoff, L., Bertran, C., Peña-Cortés, F., Hauenstein, E., Valderrama, A., Lizana, C., & Fierro, P. (2014). Accumulation of potentially toxic elements in sediments in Budi Lagoon, Araucania Region, Chile. Environment and Earth Science, 72, 4283–4290.

    Article  CAS  Google Scholar 

  • Utmazian, M. N. D. S., 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(1), 155–165.

    Article  Google Scholar 

  • Valderrama, A., Tapia, J., Peñailillo, P., & Carvajal, D. E. (2013). Water phytoremediation of cadmium and copper using Azolla filiculoides Lam. in a hydroponic system. Water Environment Journal, 27(3), 293–300.

    CAS  Google Scholar 

  • Vangronsveld, J., Herzig, R., Weyens, N., Boulet, J., Adriaensen, K., Ruttens, A., Thewys, T., Vassilev, A., Meers, E., Nehnevajova, E., Mench, M., & Van der Lelie, D. (2009). Phytoremediation of contaminated soils and groundwater: lessons from the field. Environemental Science and Pollution Research, 16(7), 765–794.

    Article  CAS  Google Scholar 

  • Walinga, I., Van der Lee, J. J., Houba, V. J. G., Van Vark, W., & Novozamsky, I. (1995). Plant analysis manual. Dordrecht: Kluwer Academia Publishers 253p.

    Book  Google Scholar 

  • Wang, Y., & Greger, M. (2004). Clonal differences in mercury tolerance, accumulation, and distribution in willow. Journal of Environmental Quality, 33(5), 1779–1785.

    Article  CAS  Google Scholar 

  • Xiong, Z. T., & Wang, H. (2005). Copper toxicity and bioaccumulation in Chinese cabbage (Brassica pekinensis Rupr.) Environmental Toxicology, 20(2), 188–194.

    Article  CAS  Google Scholar 

  • Zhivotovsky, O. P., Kuzovkina, J. A., Schulthess, C. P., Morris, T., Pettinelli, D., & Ge, M. (2010). Hydroponic screening of willows (Salix L.) for lead tolerance and accumulation. International Journal of Phytoremediation, 13(1), 75–94.

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Interdisciplinary Excellence in Research Program (PIEI) (Quimica y Bio-organica en Recursos Naturales), Universidad de Talca, and CONICYT/FONDAP/15130015. J. Cornejo thanks the CONICYT Scholarship Program for supporting his Ph.D. studies at the University of Talca (CONICYT PCHA/Doctorado Nacional/21130236).

Author information

Authors and Affiliations

  1. Institute of Natural Resources Chemistry, Universidad de Talca, 2 Norte 685, P.O. Box 747, Talca, Chile

    Jorge Cornejo & Jaime Tapia

  2. Institute of Biological Sciences, Universidad de Talca, P.O. Box 747, Talca, Chile

    Jorge Cornejo, Marco Yáñez, Ricardo Baettig & Jorge Guajardo

  3. Faculty of Forestry Sciences, Poplar Technology Center, Universidad de Talca, P.O. Box 747, Talca, Chile

    Fernando Guerra

  4. Institute of Mathematics and Physics, Universidad de Talca, P.O. Box 747, Talca, Chile

    Eduardo Alarcón

  5. Environmental Biotechnology and Engineering Group (GIBA-UDEC), Faculty of Environmental Sciences and EULA-Chile Center, Universidad de Concepción, P.O. Box 160-C, Concepcion, Chile

    Gladys Vidal

Authors
  1. Jorge Cornejo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jaime Tapia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fernando Guerra
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marco Yáñez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ricardo Baettig
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jorge Guajardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Eduardo Alarcón
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Gladys Vidal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jorge Cornejo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cornejo, J., Tapia, J., Guerra, F. et al. Variation in Copper Accumulation at the Tissue Level of Five Hybrid Poplars Subjected to Copper Stress. Water Air Soil Pollut 228, 212 (2017). https://doi.org/10.1007/s11270-017-3384-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-017-3384-7

Keywords

Search

Navigation