Abstract
Plants used for phytoextraction of heavy metals from contaminated soils with high levels of salinity should be able to accumulate heavy metals and also be tolerant to salinity. Australian native halophyte species Carpobrotus rossii has recently been shown to tolerate and accumulate multiple heavy metals, especially cadmium (Cd). This study examined the effects of salt type and concentration on phytoextraction of Cd in C. rossii. Plants were grown in contaminated soil for 63 days. The addition of salts increased plant growth and enhanced the accumulation of Cd in shoots up to 162 mg kg−1 which almost doubled the Cd concentration (87 mg kg−1) in plants without salt addition. The increased Cd accumulation was ascribed mainly to increased ionic strength in soils due to the addition of salts and resultantly increased the mobility of Cd. In comparison, the addition of Cl− resulted in 8–60 % increase in Cd accumulation in shoots than the addition of SO4 2− and NO3 −. The findings suggest that C. rossii is a promising candidate in phytoextraction of Cd-polluted soils with high salinity levels.
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References
Acosta JA, Jansen B, Kalbitz K, Faz A, Martinez-Martinez S (2011) Salinity increases mobility of heavy metals in soils. Chemosphere 85:1318–1324
Ayanaba A, KangUrea BT (1976) Urea transformation in some tropical soils. Soil Biol Biochem 8:313–316
Bolan NS, Syers JK, Tillman RW (1986) Ionic strength effects on surface charge and adsorption of phosphate and sulphate by soils. J Soil Sci 37:379–388
Broadhurst CL, Chaney RL, Davis AP, Cox A, Kumar K, Reeves RD, Green CE (2015) Growth and cadmium phytoextraction by Swiss chard, maize, rice, Noccaea caerulescens, and Alyssum murale in pH adjusted biosolids amended soils. Int J Phytoremediation 17:25–39
Brooks RR, Lee J, Reeves RD, Jaffre T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57
Chai MW, Shi FC, Li RL, Liu FC, Qiu GY, Liu LM (2013) Effect of NaCl on growth and Cd accumulation of halophyte Spartina alterniflora under CdCl2 stress. South Afri J Bot 85:63–69
de Livera J, McLaughlin MJ, Hettiarachchi GM, Kirby JK, Beak DG (2011) Cadmium solubility in paddy soils: effects of soil oxidation, metal sulfides and competitive ions. Sci Total Environ 409:1489–1497
Elzinga EJ, Sparks DL (2002) X-ray absorption spectroscopy study of the effects of pH and ionic strength on Pb(II) sorption to amorphous silica. Environ Sci Technol 36:4352–4357
Gabrijel O, Davor R, Zed R, Marija R, Monika Z (2009) Cadmium accumulation by muskmelon under salt stress in contaminated organic soil. Sci Total Environ 407:2175–2182
Geraghty DP, Ahuja KDK, Pittaway J, Shing C, Jacobson GA, Jager N, Jurkovic S, Narkowicz C, Saunders CI, Ball M, Pinkard A, Vennavaram RR, Adams MJ (2011) In vitro antioxidant, antiplatelet and anti-inflammatory activity of Carpobrotus rossii (pigface) extract. J Ethnopharmacol 134:97–103
Ghnaya T, Slama I, Messedi D, Grignon C, Ghorbel MH, Abdelly C (2007) Cd-induced growth reduction in the halophyte Sesuvium portulacastrum is significantly improved by NaCl. J Plant Res 120:309–316
Girling CA, Peterson PJ (1981) The significance of the cadmium species in uptake and metabolism of cadmium in crop plants. J Plant Nutr 3:707–720
Gonzalez-Silva BM, Briones-Gallardo R, Razo-Flores E, Celis LB (2009) Inhibition of sulfate reduction by iron, cadmium and sulfide in granular sludge. J Hazard Mater 172:400–407
Han RM, Lefevre I, Ruan CJ, Qin P, Lutts S (2012) NaCl differently interferes with Cd and Zn toxicities in the wetland halophyte species Kosteletzkya virginica (L.) Presl. Plant Growth Regul 68:97–109
Hassan MJ, Wang ZQ, Zhang GP (2005) Sulfur alleviates growth inhibition and oxidative stress caused by cadmium toxicity in rice. J Plant Nutr 28:1785–1800
Helal HM, Haque SA, Ramadan AB, Schnug E (1996) Salinity-heavy metal interactions as evaluated by soil extraction and plant analysis. Commun Soil Sci Plant Anal 27:1355–1361
Helal HM, Upenov A, Issa GJ (1999) Growth and uptake of Cd and Zn by Leucaena leucocephala in reclaimed soils as affected by NaCl salinity. J Plant Nutr Soil Sci 162:589–592
Hogan GD, Rauser WE (1981) Role of copper-binding, absorption, and translocation in copper tolerance of Agrostis gigantea Roth. J Exp Bot 32:27–36
Iqbal M, Puschenreiter M, Oburger E, Santner J, Wenzel WW (2012) Sulfur-aided phytoextraction of Cd and Zn by Salix smithiana combined with in situ metal immobilization by gravel sludge and red mud. Environ Pollut 170:222–231
John MK (1976) Interrelationships between plant cadmium and uptake of some other elements from culture solutions by oats and lettuce. Environ Pollut 11:85–95
Jordan FL, Robin-Abbott M, Maier RM, Glenn EP (2002) A comparison of chelator-facilitated metal uptake by a halophyte and a glycophyte. Environ Toxicol Chem 21:2698–2704
Kim YY, Yang YY, Lee Y (2002) Pb and Cd uptake in rice roots. Physiol Plantarum 116:368–372
Koren Š, Arčon I, Kump P, Nečemer M, Vogel-Mikuš K (2013) Influence of CdCl2 and CdSO4 supplementation on Cd distribution and ligand environment in leaves of the Cd hyperaccumulator Noccaea (Thlaspi) praecox. Plant Soil 370:125–148
Lefèvre I, Marchal G, Meerts P, Corréal E, Lutts S (2009) Chloride salinity reduces cadmium accumulation by the Mediterranean halophyte species Atriplex halimus L. Environ Exp Bot 65:142–152
Lopez-Chuken UJ, Young SD (2005) Plant screening of halophyte species for cadmium phytoremediation. Zeitschrift Fur Naturforschung 60:236–243
Lores EM, Pennock JR (1998) The effect of salinity on binding of Cd, Cr, Cu and Zn to dissolved organic matter. Chemosphere 37:861–874
McLaughlin MJ, Tiller KG, Naidu R, Stevens DP (1996) Review: The behaviour and environmental impact of contaminants in fertilizers. Aust J Soil Res 34:1–54
McLaughlin MJ, Lambrechts RM, Smolders E, Smart MK (1998) Effects of sulfate on cadmium uptake by Swiss chard: II. Effects due to sulfate addition to soil. Plant Soil 202:217–222
Mitchell LG, Grant CA, Racz GJ (2000) Effect of nitrogen application on concentration of cadmium and nutrient ions in soil solution and in durum wheat. Can J Soil Sci 80:107–115
Monsant AC, Tang C, Baker AJ (2008) The effect of nitrogen form on rhizosphere soil pH and zinc phytoextraction by Thlaspi caerulescens. Chemosphere 73:635–642
Muhling KH, Lauchli A (2003) Interaction of NaCl and Cd stress on compartmentation pattern of cations, antioxidant enzymes and proteins in leaves of two wheat genotypes differing in salt tolerance. Plant Soil 253:219–231
Nanda-Kumar PBA, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238
Ondrasek G, Rengel Z, Romic D, Savic R (2012) Salinity decreases dissolved organic carbon in the rhizosphere and increases trace element phyto-accumulation. Eur J Soil Sci 63:685–693
Oporto C, Smolders E, Degryse F, Verheyen L, Vandecasteele C (2009) DGT-measured fluxes explain the chloride-enhanced cadmium uptake by plants at low but not at high Cd supply. Plant Soil 318:127–135
Ozkutlu F, Turan M (2013) Soil salinity increase cd uptake of lettuce (Lattuca sativa L.). Carpath J Earth Env 8:97–106
Pirie A, Parsons D, Renggli J, Narkowicz C, Jacobson GA, Shabala S (2013) Modulation of flavonoid and tannin production of Carpobrotus rossii by environmental conditions. Environ Exp Bot 87:19–31
Prasad MNV, Sajwan KS, Naidu R (2006) Trace elements in the environment: biogeochemistry, biotechnology, and bioremediation. Taylor & Francis Group, LLC
Schwartz C, Echevarria G, Morel JL (2003) Phytoextraction of cadmium with Thlaspi caerulescens. Plant Soil 249:27–35
Sirguey C, Ouvrard S (2013) Contaminated soils salinity, a threat for phytoextraction? Chemosphere 91:269–274
Wali M, Fourati E, Hmaeid N, Ghabriche R, Poschenrieder C, Abdelly C, Ghnaya T (2015) NaCl alleviates Cd toxicity by changing its chemical forms of accumulation in the halophyte Sesuvium portulacastrum. Environ Sci Pollut Res 22:10769–10777
Weggler-Beaton K, McLaughlin MJ, Graham RD (2000) Salinity increases cadmium uptake by wheat and Swiss chard from soil amended with biosolids. Aust J Soil Res 38:37–45
Wenzel WW, Bunkowski M, Puschenreiter M, Horak O (2003) Rhizosphere characteristics of indigenously growing nickel hyperaccumulator and excluder plants on serpentine. Environ Pollut 123:131–138
Xie HL, Jiang RF, Zhang FS, McGrath SP, Zhao FJ (2009) Effect of nitrogen form on the rhizosphere dynamics and uptake of cadmium and zinc by the hyperaccumulator Thlaspi caerulescens. Plant Soil 318:205–215
Xu J, Yin H, Liu X, Li X (2011) Salt affects plant Cd-stress responses by modulating growth and Cd accumulation. Planta 231:449–459
Zhang C, Sale PW, Doronila AI, Clark GJ, Livesay C, Tang C (2014) Australian native plant species Carpobrotus rossii (Haw.) Schwantes shows the potential of cadmium phytoremediation. Environ Sci Pollut Res 21:9843–9851
Zhang C, Sale PW, Clark GJ, Doronila AI, Tang C (2015) Succulent species differ substantially in their tolerance and phytoextraction potential when grown in the combinations of Cd, Cr, Cu, Mn, Ni, Pb and Zn. Environ Sci Pollut Res 22:18824–18838
Zhao ZQ, Zhu YG, Li HY, Smith SE, Smith FA (2004) Effects of forms and rates of potassium fertilizers on cadmium uptake by two cultivars of spring wheat (Triticum aestivum, L.). Environ Int 29:973–978
Zurayk RA, Khoury NF, Talhouk SN, Baalbaki RZ (2001) Salinity-heavy metal interactions in four salt-tolerant plant species. J Plant Nutrition 24:1773–1786
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This research was supported by an Australian Research Council Linkage Project (LP100100800).
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Zhang, C., Sale, P.W.G. & Tang, C. Cadmium uptake by Carpobrotus rossii (Haw.) Schwantes under different saline conditions. Environ Sci Pollut Res 23, 13480–13488 (2016). https://doi.org/10.1007/s11356-016-6508-5
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DOI: https://doi.org/10.1007/s11356-016-6508-5