Skip to main content
Log in

Variations of cadmium tolerance and accumulation among 39 Salix clones: implications for phytoextraction

  • Original Article
  • Published:
Environmental Earth Sciences Aims and scope Submit manuscript

Abstract

Willows (Salix spp.) show large remediation potential for cadmium (Cd)-contaminated sites, with Cd phytoextraction capacity significantly varying among specie and clone levels. In this study, a relatively large number of willow clones (39 clones) from China were evaluated for the differences in Cd tolerance and accumulation exposed to 10 μM CdCl2 by hydroponic system for 35 days. The clones showed a wide variation of biomass accumulation ranging from growth inhibition to stimulation. Shoot tolerance indexes (TIs) varied between 0.09 and 1.85, and root TIs varied between 0.27 and 1.99 among clones. The large differences in Cd concentration (μg g−1 dry weight, DW) ranged from 64.7 to 663.7 in leaves, from 118.0 to 308.4 in stems, and from 163.9 to 1,426.4 in roots among clones. Leaf translocation factors (TFs) differed from 0.09 to 1.72 and shoot TFs differed from 0.15 to 1.08. Total Cd content of shoots (including leaves and stems) varied between 29.8 and 2,726.52 μg plant−1 DW among clones. With respect to TIs, TFs, Cd concentration, and shoot Cd content, the five clones showed higher Cd phytoextraction potential than the other clones. The results support that the selection of willows with enhanced phytoremediation efficiency should be concentrated on the clone level.

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

  • Bert V, Meerts P, Saumitou-Laprade P, Salis P, Gruber W, Verbruggen N (2003) Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri. Plant Soil 249:9–18

    Article  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. Environ Exp Bot 62:290–299

    Article  Google Scholar 

  • Castillo-Michel HA, Hernandez N, Martinez-Martinez A, Parsons JG, Peralta-Videa JR, Gardea-Torresdey JL (2009) Coordination and speciation of cadmium in corn seedlings and its effects on macro-and micronutrients uptake. Plant Physiol Biochem 47:608–614

    Article  Google Scholar 

  • Cosio C, Vollenweider P, Keller C (2006) Localization and effects of cadmium in leaves of a cadmium-tolerant willow (Salix viminalis L.): I. Macrolocalization and phytotoxic effects of cadmium. Environ Exp Bot 58:64–74

    Article  Google Scholar 

  • Deng DM, Shu WS, Zhang J, Zou HL, Lin Z, Ye ZH, Wong MH (2007) Zinc and cadmium accumulation and tolerance in populations of Sedum alfredii. Environ Pollut 147:381–386

    Article  Google Scholar 

  • Deram A, Denayer FO, Dubourgier HC, Douay F, Petit D, Van Haluwyn C (2007) Zinc and cadmium accumulation among and within populations of the pseudometalophytic species Arrhenatherum elatius: implications for phytoextraction. Sci Total Environ 372:372–381

    Article  Google Scholar 

  • Dos Santos Utmazian MN, Wenzel WW (2007) Cadmium and zinc accumulation in willow and poplar species grown on polluted soils. J Plant Nutr Soil Sci 170:265–272

    Article  Google Scholar 

  • Dos Santos Utmazian MN, Wieshammer G, Vega R, Wenzel WW (2007) Hydroponic screening for metal resistance and accumulation of cadmium and zinc in twenty clones of willows and poplars. Environ Pollut 148:155–165

    Article  Google Scholar 

  • Doumett S, Lamperi L, Checchini L, Azzarello E, Mugnai S, Mancuso S, Petruzzelli G, Del Bubba M (2008) Heavy metal distribution between contaminated soil and Paulownia tomentosa, in a pilot-scale assisted phytoremediation study: influence of different complexing agents. Chemosphere 72:1481–1490

    Article  Google Scholar 

  • Greger M, Landberg T (1999) Use of willow in phytoextraction. Int J Phytoremediation 1:115–123

    Article  Google Scholar 

  • Haque N, Peralta-Videa JR, Jones GL, Gill TE, Gardea-Torresdey JL (2008) Screening the phytoremediation potential of desert broom (Baccharis sarothroides Gray) growing on mine tailings in Arizona, USA. Environ Pollut 153:362–368

    Article  Google Scholar 

  • Hernández-Allica J, Becerril JM, Garbisu C (2008) Assessment of the phytoextraction potential of high biomass crop plants. Environ Pollut 152:32–40

    Article  Google Scholar 

  • Karp A, Hanley SJ, Trybush SO, Macalpine W, Pei M, Shield I (2011) Genetic improvement of willow for bioenergy and biofuelsfree access. J Integr Plant Biol 53:151–165

    Article  Google Scholar 

  • Keoleian GA, Volk TA (2005) Renewable energy from willow biomass crops: life cycle energy, environmental and economic performance. Crit Rev Plant Sci 24:385–406

    Article  Google Scholar 

  • Khasa PD, Hambling B, Kernaghan G, Fung M, Ngimbi E (2002) Genetic variability in salt tolerance of selected boreal woody seedlings. Forest Ecol Manag 165:257–269

    Article  Google Scholar 

  • Klang-Westin E, Perttu K (2002) Effects of nutrient supply and soil cadmium concentration on cadmium removal by willow. Biomass Bioenerg 23:415–426

    Article  Google Scholar 

  • Kuzovkina YA, Quigley MF (2005) Willows beyond wetlands: uses of Salix L. species for environmental projects. Water Air Soil Poll 162:183–204

    Article  Google Scholar 

  • Kuzovkina YA, Knee M, Quigley MF (2004) Cadmium and copper uptake and translocation in five willow (Salix L.) species. Int J Phytoremediation 6:269–287

    Article  Google Scholar 

  • Landberg T, Greger M (2002) Interclonal variation of heavy metal interactions in Salix viminalis. Environ Toxicol Chem 21:2669–2674

    Article  Google Scholar 

  • Licht LA, Isebrands JG (2005) Linking phytoremediated pollutant removal to biomass economic opportunities. Biomass Bioenerg 28:203–218

    Article  Google Scholar 

  • 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. Physiol Plant 120:537–545

    Article  Google Scholar 

  • Meers E, Vandecasteele B, Ruttens A, Vangronsveld J, Tack FMG (2007) Potential of five willow species (Salix spp.) for phytoextraction of heavy metals. Environ Exp Bot 60:57–68

    Article  Google Scholar 

  • Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178

    Google Scholar 

  • Mirck J, Isebrands JG, Verwijst T, Ledin S (2005) Development of short-rotation willow coppice systems for environmental purposes in Sweden. Biomass Bioenerg 28:219–228

    Article  Google Scholar 

  • Mleczek M, Kaczmarek Z, Magdziak Z, Golinski PK (2010) Hydroponic estimation of heavy metal accumulation by different genotypes of Salix. J Environ Sci Heal A 45:569–578

    Article  Google Scholar 

  • Pietrini F, Zacchini M, Iori V, Pietrosanti L, Bianconi D, Massacci A (2009) Screening of poplar clones for cadmium phytoremediation using photosynthesis, biomass and cadmium content analyses. Int J Phytoremediat 12:105–120

    Article  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 Biol 12:355–363

  • Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees—a review. Environ Int 29:529–540

    Article  Google Scholar 

  • Punshon T, Dickinson NM (1997) Acclimation of Salix to metal stress. New Phytol 137:303–314

    Article  Google Scholar 

  • Punshon T, Lepp NW, Dickinson NM (1995) Resistance to copper toxicity in some British willows. J Geochem Explor 52:259–266

    Article  Google Scholar 

  • Purdy JJ, Smart LB (2008) Hydroponic screening of shrub willow (Salix spp.) for arsenic tolerance and uptake. Int J Phytoremediation 10:515–528

    Article  Google Scholar 

  • Rockwood DL, Naidu CV, Carter DR, Rahmani M, Spriggs TA, Lin C, Alker GR, Isebrands JG, Segrest SA (2004) Short-rotation woody crops and phytoremediation: opportunities for agroforestry? Agroforest Syst 1–3:51–63

    Google Scholar 

  • Shanahan JO, Brummer JE, Leininger WC, Paschke MW (2007) Manganese and zinc toxicity thresholds for mountain and Geyer willow. Int J Phytoremediation 9:437–452

    Article  Google Scholar 

  • Smiri M, Chaoui A, El Ferjani E (2009) Respiratory metabolism in the embryonic axis of germinating pea seed exposed to cadmium. J Plant Physiol 166:259–269

    Article  Google Scholar 

  • Stolt P, Asp H, Hultin S (2006) Genetic variation in wheat cadmium accumulation on soils with different cadmium concentrations. J Agron Crop Sci 192:201–208

    Article  Google Scholar 

  • Tlustoš P, Száková JI, Vysloužilová M, Pavlíková D, Weger J, Javorská H (2007) Variation in the uptake of arsenic, cadmium, lead, and zinc by different species of willows Salix spp. grown in contaminated soils. Cent Eur J Biol 2:254–275

    Article  Google Scholar 

  • Usman ARA, Lee SS, Awad YM, Lim KJ, Yang JE, Ok YS (2012) Soil pollution assessment and identification of hyperaccumulating plants in chromated copper arsenate (CCA) contaminated sites, Korea. Chemosphere 87:872–887

    Article  Google Scholar 

  • Usman ARA, Almaroai YA, Ahmad M, Vithanage M, Sik Ok YS (2013) Toxicity of synthetic chelators and metal availability in poultry manure amended Cd, Pb and As contaminated agricultural soil. J Hazard Mater 262:1022–1030

    Article  Google Scholar 

  • Van Nevel L, Mertens J, Staelens J, De Schrijver A, Tack FMG, De Neve S, Meers E, Verheyen K (2011) Elevated Cd and Zn uptake by aspen limits the phytostabilization potential compared to five other tree species. Ecol Eng 37:1072–1080

    Article  Google Scholar 

  • Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794

    Article  Google Scholar 

  • Wang Y, Greger M (2004) Clonal differences in mercury tolerance, accumulation, and distribution in willow. J Environ Qual 33:1779–1785

    Article  Google Scholar 

  • Watson C, Pulford ID, Riddell-Black D (2003a) Development of a hydroponic screening technique to assess heavy metal resistance in willow (Salix). Int J Phytoremediation 5:333–349

    Article  Google Scholar 

  • Watson C, Pulford ID, Riddell-Black D (2003b) Screening of willow species for resistance to heavy metals: comparison of performance in a hydroponics system and field trials. Int J Phytoremediation 5:351–365

    Article  Google Scholar 

  • Xue D, Chen M, Zhang G (2009) Mapping of QTLs associated with cadmium tolerance and accumulation during seedling stage in rice (Oryza sativa L.). Euphytica 165:587–596

    Article  Google Scholar 

  • Ying R-R, Qiu R-L, Tang Y-T, Hu P-J, Qiu H, Chen H-R, Shi T-H, Morel J-L (2010) Cadmium tolerance of carbon assimilation enzymes and chloroplast in Zn/Cd hyperaccumulator Picris divaricata. J Plant Physiol 167:81–87

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Zeng F, Mao Y, Cheng W, Wu F, Zhang G (2008) Genotypic and environmental variation in chromium, cadmium and lead concentrations in rice. Environ Pollut 153:309–314

    Article  Google Scholar 

  • Zhang Z, Rengel Z, Meney K (2010) Cadmium accumulation and translocation in four emergent wetland species. Water Air Soil Poll 212:239–249

    Article  Google Scholar 

  • Zhivotovsky OP, Kuzovkina JA, Schulthess CP, Morris T, Pettinelli D, Ge M (2010) hydroponic screening of willows (Salix L.) for lead tolerance and accumulation. Int J Phytoremediat 13:75–94

    Article  Google Scholar 

Download references

Acknowledgments

This work was funded by the Natural Science Foundation of China (Grant No. 31100513), the Key International Cooperative Project of CN-USA (Grant No. 2010DFB33960), the Key Project from Zhejiang Science and Technology Bureau (Grant No. 2011C13015), the Key Project of Ministry of Science and Technology of China (Grant No. 2012BAC17B02) and the Fundamental Research Funds for the Central Universities. We thank Zhang Huaxian for providing excellent technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaoe Yang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, W., Zhao, F., Zhang, X. et al. Variations of cadmium tolerance and accumulation among 39 Salix clones: implications for phytoextraction. Environ Earth Sci 73, 3263–3274 (2015). https://doi.org/10.1007/s12665-014-3636-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12665-014-3636-4

Keywords

Navigation