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Metal Tolerance, Accumulation and Translocation in Poplar and Willow Clones Treated with Cadmium in Hydroponics

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To evaluate the phytoremediation capability of some poplar and willow clones a hydroponic screening for cadmium tolerance, accumulation and translocation was performed. Rooted cuttings were exposed for 3 weeks to 50 μM cadmium sulphate in a growth chamber and morpho-physiological parameters and cadmium content distribution in various parts of the plant were evaluated. Total leaf area and root characteristics in clones and species were affected by cadmium treatment in different ways. Poplar clones showed a remarkable variability whereas willow clones were observed to be more homogeneous in cadmium accumulation and distribution. This behaviour was further confirmed by the calculation of the bio-concentration factor (BCF) and the translocation factor (Tf). Mean values of all the clones of the two Salicaceae species showed that willows had a far greater ability to tolerate cadmium than poplars, as indicated by the tolerance index (Ti), calculated on the dry weight of roots and shoots of plants. As far as the mean values of Tf was concerned, the capacity of willows to translocate was double that of poplars. On the contrary, the mean values of total BCF in poplar clones was far higher with respect to those in willows. The implications of these results in the selection of Salicaceae clones for phytoremediation purposes were discussed.

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  1. Ait Ali, N., Pilar Bernal, M., & Ater, M. (2004). Tolerance and bioaccumulation of cadmium by Phragmites australis grown in the presence of elevated concentrations of cadmium, copper and zinc. Aquatic Botany, 80, 163–176. doi:10.1016/j.aquabot.2004.08.008.

  2. Arnon, D. I., & Hoagland, D. R. (1940). Crop production in artificial culture solutions and in soils with special reference to factors influencing yields and absorption of inorganic nutrient. Soil Science, 50, 463–483.

  3. Becerril, J. M., Munoz-Rueda, A., Aparicio-Tejo, P., & Gonzales-Murua, C. (1988). The effects of cadmium and lead on photosynthetic electron transport in clover and lucerne. Plant Physiology and Biochemistry, 26, 357–363.

  4. Ceulemans, R., Scarascia-Mugnozza, G., Wiard, B. M., Braatne, J. H., Hinckley, T. M., Stettler, R. F., et al. (1992). Production physiology and morphology of Populus species and their hybrids grown under short rotation. I. Clonal comparisons of 4-year growth and phenology. Canadian Journal of Forest Research, 22, 1937–1948.

  5. Cunningham, S. D., & Ow, D. W. (1996). Promises and prospects of phytoremediation. Plant Physiology, 110, 715–719.

  6. Deng, H., Ye, Z. H., & Wong, M. H. (2004). Accumulation of lead, zinc, copper and cadmium by 12 wetland plant species thriving in metal-contaminated sites in China. Environmental Pollution, 132, 29–40. doi:10.1016/j.envpol.2004.03.030.

  7. Dickinson, N. M., & Pulford, I. D. (2005). Cadmium phytoextraction using short-rotation coppice Salix: The evidence trail. Environment International, 31, 609–613. doi:10.1016/j.envint.2004.10.013.

  8. 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. doi:10.1016/j.envpol.2006.10.045.

  9. Fischerová, Z., Tlustos, P., Szakova, J., & Sichorova, K. (2006). A comparison of phytoremediation capability of selected plant species for given trace elements. Environmental Pollution, 144, 93–100. doi:10.1016/j.envpol.2006.01.005.

  10. Greger, M., & Landberg, T. (1999). Use of willow in phytoextraction. International Journal of Phytoremediation, 1, 115–123. doi:10.1080/15226519908500010.

  11. Keltjens, W. G., & van Beusichem, M. L. (1998). Phytochelatins as biomarkers for heavy metal stress in maize (Zea mays L.) and wheat (Triticum aestivum L.): Combined effects of copper and cadmium. Plant and Soil, 203, 119–126. doi:10.1023/A:1004373700581.

  12. Kramer, U., Cotter-Howells, J. D., Charnock, J. M., Baker, A. J. M., & Smith, J. A. C. (1996). Free histidine as a metal chelator in plants that accumulate nickel. Nature, 379, 635–638. doi:10.1038/379635a0.

  13. Kumar, P. B. A. N., Dushenkov, V., Motto, H., & Raskin, I. (1995). Phytoextraction: The use of plants to remove heavy metals from soils. Environmental Science & Technology, 29, 1232–1238. doi:10.1021/es00005a014.

  14. 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, 269–287. doi:10.1080/16226510490496726.

  15. Kuzovkina, Y. A., & Quigley, M. F. (2005). Willows beyond wetlands: Uses of Salix L. species for environmental projects. Water, Air, and Soil Pollution, 162, 183–204. doi:10.1007/s11270-005-6272-5.

  16. Landberg, T., & Greger, M. (1996). Differences in uptake and tolerance to heavy metals in Salix from unpolluted and polluted areas. Applied Geochemistry, 11, 175–180. doi:10.1016/0883-2927(95)00082-8.

  17. Laureysens, I., Blust, R., De Temmerman, L., Lemmens, C., & Ceulemans, R. (2004a). 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, 485–494. doi:10.1016/j.envpol.2004.02.009.

  18. Laureysens, I., Bogaert, J., Blust, R., & Ceulemans, R. (2004b). Biomass production of 17 poplar clones in a short-rotation coppice culture on a waste disposal site and its relation to soil characteristics. Forest Ecology and Management, 187, 295–309. doi:10.1016/j.foreco.2003.07.005.

  19. Lunáčková, L., Masarovičová, E., Králová, K., & Streško, V. (2003a). Response of fast growing woody plants from family Salicaceae to cadmium treatment. Bulletin of Environmental Contamination and Toxicology, 70, 576–585. doi:10.1007/s00128-003-0024-2.

  20. Lunáčková, L., Šottníková, A., Masarovičová, E., Lux, A., & Streško, V. (2003b). Comparison of cadmium effect on willow and poplar in response to different cultivation conditions. Biologia Plantarum, 47, 403–411. doi:10.1023/B:BIOP.0000023884.54709.09.

  21. Lux, A., Šottníková, A., Opatrná, J., & Greger, M. (2004). Differences in structure of adventitious roots in Salix clones with contrasting characteristics of cadmium accumulation and sensitivity. Physiologia Plantarum, 120, 537–545. doi:10.1111/j.0031-9317.2004.0275.x.

  22. 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. doi:10.1023/B:WATE.0000044862.51031.fb.

  23. Mattina, M. J. I., Lannucci-Berger, W., Musante, C., & White, J. C. (2003). Concurrent plant uptake of heavy metals and persistent organic pollutants from soil. Environmental Pollution, 124, 375–378. doi:10.1016/S0269-7491(03)00060-5.

  24. Mills, T. M., Robinson, B. H., Green, S., Clothier, B., Fung, L. E., & Hurst, S. (2000). Difference in Cd uptake and distribution within poplar and willow species. In Proceedings of the 42nd Annual Conference and Expo of the New Zealand Water and Waste Association, Rotorua, New Zealand.

  25. Padmavathiamma, P. K., & Li, L. Y. (2007). Phytoremediation technology: Hyper-accumulation metals in plants. Water, Air, and Soil Pollution, 184, 105–126. doi:10.1007/s11270-007-9401-5.

  26. Perttu, K. L. (1999). Environmental and hygienic aspects of willow coppice in Sweden. Biomass and Bioenergy, 16, 291–297. doi:10.1016/S0961-9534(98)00012-9.

  27. Pietrini, F., Iannelli, M. A., Montanari, R., Bianconi, D., & Massacci, A. (2005). Cadmium interaction with thiols and photosynthesis in higher plants. In A. Hemantaranjan (Ed.), Advances in plant physiology (pp. 313–326). Jodhpur, India: Scientific Publishers.

  28. Pietrini, F., Iannelli, M. A., Pasqualini, S., & Massacci, A. (2003). Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex strudel. Plant Physiology, 133, 829–837. doi:10.1104/pp.103.026518.

  29. Pilipović, A., Nikolić, N., Orlović, S., Petrović, N., & Krstić, B. (2005). Cadmium phytoextraction potential of poplar clones (Populus spp.). Zeitschrift für Naturforschung, 60c, 247–251.

  30. Pulford, I. D., Riddell-Black, D., & Stewart, C. (2002). Heavy metal uptake by willow clones from sewage sludge-treated soil: The potential for phytoremediation. International Journal of Phytoremediation, 4, 59–72. doi:10.1080/15226510208500073.

  31. Pulford, I. D., & Watson, C. (2003). Phytoremediation of heavy metal-contaminated land by trees – A review. Environment International, 29, 529–540. doi:10.1016/S0160-4120(02)00152-6.

  32. Punshon, T., & Dickinson, N. M. (1999). Heavy metal resistance and accumulation characteristics in willows. International Journal of Phytoremediation, 1, 361–385. doi:10.1080/15226519908500025.

  33. Raskin, I., Smith, R. D., & Salt, D. E. (1997). Phytoremediation of metals: Using plants to remove pollutants from the environment. Current Opinion in Biotechnology, 2, 221–226. doi:10.1016/S0958-1669(97)80106-1.

  34. Rauser, W. E. (1999). Structure and function of metal chelators produced by plants – The case for organic acids, amino acids, phytin, and metallothioneins. Cell Biochemistry and Biophysics, 31, 19–48. doi:10.1007/BF02738153.

  35. Rauser, W. E., & Muwly, P. (1995). Retention of cadmium in roots of maize seedlings. Role of complexation by phytochelatins and related thiol peptides. Plant Physiology, 109, 195–202. doi:10.1104/pp.109.1.195.

  36. Riddell-Black, D. (1994). Heavy metal uptake by fast growing willow species. In P. Aronsson, & K. Perttu (Eds.), Willow vegetation filters for municipal wastewaters and sludges. A biological purification system (pp. 145–151). Uppsala, Sweden: Department of Ecology and Environmental Research, Section of Short Rotation Forestry.

  37. Robinson, B. H., Mills, T. M., Green, S., Chancerel, B., Clothier, B., Fung, L. E., et al. (2005). Trace element accumulation by poplars and willows used for stock fodder. New Zeland Journal of Agriculture Research, 48, 489–497.

  38. Robinson, B. H., Mills, T. M., Petit, D., Fung, L. E., Green, S., & Clothier, B. (2000). Natural and induced cadmium-accumulation in poplar and willow: Implications for phytoremediation. Plant and Soil, 227, 301–306. doi:10.1023/A:1026515007319.

  39. Rockwood, D. L., Naidu, C. V., Carter, D. R., Rahmani, M., Spriggs, T. A., Lin, C., et al. (2004). Short-rotation woody crops and phytoremediation: Opportunities for agroforestry? Agroforestry Systems, 61, 51–63. doi:10.1023/B:AGFO.0000028989.72186.e6.

  40. Rosselli, W., Keller, C., & Boschi, K. (2003). Phytoextraction capacity of trees growing on a metal contaminated soil. Plant and Soil, 256, 265–272. doi:10.1023/A:1026100707797.

  41. Sanità di Toppi, L., & Gabbrielli, R. (1999). Responses to cadmium in higher plants. Environmental and Experimental Botany, 41, 105–130. doi:10.1016/S0098-8472(98)00058-6.

  42. Scarascia-Mugnozza, G., Ceulemans, R., Heilman, P. E., Isebrands, J. G., Stettler, R. F., & Hinckley, T. M. (1997). Production physiology and morphology of Populus species and their hybrids grown under short rotation. II. Biomass components and harvest index of hybrid and parental species clones. Canadian Journal of Forest Research, 27, 285–294.

  43. Šottníková, A., Lunáčková, L., Masarovičová, E., Lux, A., & Streško, V. (2003). Changes in the rooting and growth of willow and poplars induced by cadmium. Biologia Plantarum, 46, 129–131. doi:10.1023/A:1022395118998.

  44. Unterbrunner, R., Puschenreiter, M., Sommer, P., Wieshammer, G., Tlustos, P., Zupan, M., et al. (2007). Heavy metal accumulation in tree growing on contaminated sites in Central Europe. Environmental Pollution, 148, 107–114. doi:10.1016/j.envpol.2006.10.035.

  45. Wang, K. S., Huang, L. C., Lee, H. S., Chen, P. Y., & Chang, S. H. (2008). Phytoextraction of cadmium by Ipomoea aquatica (water spinach) in hydroponic solution: Effects of cadmium speciation. Chemosphere, 72, 666–672. doi:10.1016/j.chemosphere.2008.03.034.

  46. Watson, C., Pulford, I. D., & Riddell-Black, D. (1999). Heavy metal toxicity responses of two willow (Salix) varieties grown hydroponically: Development of a tolerance screening test. Environmental Geochemistry and Health, 21, 359–364. doi:10.1023/A:1006796720300.

  47. Watson, C., Pulford, I. D., & Riddell-Black, D. (2003). Screening of willow species for resistance to heavy metals: Comparison of performance in a hydroponics system and field trials. International Journal of Phytoremediation, 5, 351–365. doi:10.1080/16226510390268748.

  48. Wilkins, D. A. (1978). The measurement of tolerance to edaphic factors by means of root growth. The New Phytologist, 80, 623–633. doi:10.1111/j.1469-8137.1978.tb01595.x.

  49. Zayed, A., Gowthaman, S., & Terry, N. (1998). Phytoaccumulation of trace elements by wetlands plants: I. Duckweed. Journal of Environmental Quality, 27, 715–721.

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This work was funded by MIUR (Ministry for Education, University and Research) under PRIN 2005 project no. 2005-072892. Authors also wish to thank Prof. Paolo Sequi (CRA-RPS) for research collaboration within PRAL research project and Antonio Barchetti (CRA-RPS) for valuable technical assistance.

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Correspondence to Angelo Massacci.

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Zacchini, M., Pietrini, F., Scarascia Mugnozza, G. et al. Metal Tolerance, Accumulation and Translocation in Poplar and Willow Clones Treated with Cadmium in Hydroponics. Water Air Soil Pollut 197, 23–34 (2009). https://doi.org/10.1007/s11270-008-9788-7

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  • Bioconcentration factor
  • Cadmium
  • Hydroponic culture
  • Phytoremediation
  • Poplar
  • Translocation factor
  • Willow