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Succulent species differ substantially in their tolerance and phytoextraction potential when grown in the presence of Cd, Cr, Cu, Mn, Ni, Pb, and Zn

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Abstract

Plants for the phytoextraction of heavy metals should have the ability to accumulate high concentrations of such metals and exhibit multiple tolerance traits to cope with adverse conditions such as coexistence of multiple heavy metals, high salinity, and drought which are the characteristics of many contaminated soils. This study compared 14 succulent species for their phytoextraction potential of Cd, Cr, Cu, Mn, Ni, Pb, and Zn. There were species variations in metal tolerance and accumulation. Among the 14 succulent species, an Australian native halophyte Carpobrotus rossii exhibited the highest relative growth rate (20.6–26.6 mg plant−1 day−1) and highest tolerance index (78–93 %), whilst Sedum “Autumn Joy” had the lowest relative growth rate (8.3–13.6 mg plant−1 day−1), and Crassula multicava showed the lowest tolerance indices (<50 %). Carpobrotus rossii and Crassula helmsii showed higher potential for phytoextraction of these heavy metals than other species. These findings suggest that Carpobrotus rossii is a promising candidate for phytoextraction of multiple heavy metals, and the aquatic or semiterrestrial Crassula helmsii is suitable for phytoextraction of Cd and Zn from polluted waters or wetlands.

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References

  • Arshad M, Silvestre J, Pinelli E, Kallerhoff J, Kaemmerer M, Tarigo A, Shahid M, Guiresse M, Pradere P, Dumat C (2008) A field study of lead phytoextraction by various scented Pelargonium cultivars. Chemosphere 71:2187–2192

    Article  CAS  Google Scholar 

  • Baker AJM (1981) Accumulators and excluders—strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654

    Article  CAS  Google Scholar 

  • Baker AJM (1984) Environmentally-induced cadmium tolerance in the grass Holcus lanatus L. Chemosphere 13:585–589

    Article  CAS  Google Scholar 

  • Baker AJM, Reeves RD, Hajar ASM (1994) Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. & C. Presl (Brassicaceae). New Phytol 127:61–68

    Article  CAS  Google Scholar 

  • Baker AJ, McGrath SP, Reeves RD, Smith JAC (1999) Metal hyperaccumulator plants. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soil and water. Lewis Publishers, London, pp 85–107

    Google Scholar 

  • Bauddh K, Singh RP (2012) Growth, tolerance efficiency and phytoremediation potential of Ricinus communis (L.) and Brassica juncea (L.) in salinity and drought affected cadmium contaminated soil. Ecotoxicol Environ Saf 85:13–22

    Article  CAS  Google Scholar 

  • Baun DL, Christensen TH (2004) Speciation of heavy metals in landfill leachate: a review. Waste Manag Res 22:3–23

    Article  CAS  Google Scholar 

  • Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250

    Article  CAS  Google Scholar 

  • Blaylock MJ, Salt DE, Dushenkov S, Zakharova O, Gussman C, Kapulnik Y, Ensley BD, Raskin I (1997) Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agents. Environ Sci Technol 31:860–865

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Callahan DL, Baker AJM, Kolev SD, Wedd AG (2006) Metal ion ligands in hyperaccumulating plants. J Biol Inorg Chem 11:2–12

    Article  CAS  Google Scholar 

  • Chaney RL (1983) Plant uptake of inorganic waste constituents. In: Parr JF, Marsh PD, Kla JM. Park Ridge, NJ (eds), Land treatment of hazardous wastes. Noyes Data Corporation, pp 50–76

  • Cox RM, Hutchinson TC (1979) Metal co-tolerance in the grass Deschampsia cespitos. Nature 279:231–233

    Article  CAS  Google Scholar 

  • Cox RM, Hutchinson TC (1980) Multiple metal tolerances in the grass Deschampsia cespitosa (L.) Beauv. from the Sudbury smelting area. New Phytol 84:631–647

    Article  CAS  Google Scholar 

  • Dan TV (2001) Phytoremediation of metal contaminated soils metal tolerance and metal accumulation in Pelargonium sp. Ph. D. Thesis. The University of Guelph, Horticultural Science and Land Resource Division

  • Dan TV, KrishnaRaj S, Saxena PK (2000) Metal tolerance of scented geranium (Pelargonium sp. ‘Frensham: effects of cadmium and nickel on chlorophyll fluorescence kinetics’. Int J Phytoremed 2:91–104

    Article  CAS  Google Scholar 

  • Dan TV, KrishnaRaj S, Saxena PK (2002) Cadmium and nickel uptake and accumulation in scented geranium (Pelargonium sp. ‘Frensham’). Water Air Soil Pollut 137:355–364

    Article  CAS  Google Scholar 

  • Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol 179:318–333

    Article  CAS  Google Scholar 

  • Ebbs SD, Lasat MM, Brady DJ, Cornish J, Gordon R, Kochian LV (1997) Phytoextraction of cadmium and zinc from a contaminated soil. J Environ Qual 26:1424–1430

    Article  CAS  Google Scholar 

  • Fernando DR, Marshall AT, Forster PI, Hoebee SE, Siegele R (2013) Multiple metal accumulation within a manganese-specific genus. Am J Bot 100:690–700

    Article  CAS  Google Scholar 

  • Fitz WJ, Wenzel WW (2002) Arsenic transformations in the soil–rhizosphere–plant system: fundamentals and potential application to phytoremediation. J Biotechnol 99:259–278

    Article  CAS  Google Scholar 

  • Garbisu C, Alkorta I (2001) Phytoextraction: a cost-effective plant-based technology for the removal of metals from the environment. Bioresour Technol 77:229–236

    Article  CAS  Google Scholar 

  • Gisbert C, Clemente R, Navarro-Aviñó J, Baixauli C, Ginér A, Serrano R, Walker DJ, Bernal MP (2006) Tolerance and accumulation of heavy metals by Brassicaceae species grown in contaminated soils from Mediterranean regions of Spain. Environ Exp Bot 56:19–27

    Article  CAS  Google Scholar 

  • Gleba D, Borisjuk NV, Borisjuk LG, Kneer R, Poulev A, Sarzhinskaya M, Dushenkov S, Logendra S, Gleba YY, Raskin I (1999) Use of plant roots for phytoremediation and molecular farming. Proc Natl Acad Sci U S A 96:5973–5977

    Article  CAS  Google Scholar 

  • Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465:190–198

    Article  CAS  Google Scholar 

  • Hassan Z, Aarts MGM (2011) Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environ Exp Bot 72:53–63

    Article  CAS  Google Scholar 

  • Hu P-J, Qiu R-L, Senthilkumar P, Jiang D, Chen Z-W, Tang Y-T, Liu F-J (2009) Tolerance, accumulation and distribution of zinc and cadmium in hyperaccumulator Potentilla griffithii. Environ Exp Bot 66:317–325

    Article  CAS  Google Scholar 

  • Kochian LV, Ebbs SD (1998) Phytoextraction of zinc by oat (Avena sativa), barley (Hordeum vulgare), and Indian mustard (Brassica juncea). Environ Sci Technol 32:802–806

    Article  Google Scholar 

  • KrishnaRaj S, Dan TV, Saxena PK (2000) A fragrant solution to soil remediation. Int J Phytoremed 2:117–132

    Article  Google Scholar 

  • Kumar PBAN, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238

    Article  CAS  Google Scholar 

  • Küpper H, Gotz B, Mijovilovich A, Kupper FC, Meyer-Klaucke W (2009) Complexation and toxicity of copper in higher plants. I. Characterization of copper accumulation, speciation, and toxicity in Crassula helmsii as a new copper accumulator. Plant Physiol 151:702–714

    Article  Google Scholar 

  • Long XX, Yang XE, Ni WZ, Ye ZQ, He ZL, Calvert DV, Stoffella JP (2003) Assessing zinc thresholds for phytotoxicity and potential dietary toxicity in selected vegetable crops. Commun Soil Sci Plant Anal 34:1421–1434

    Article  CAS  Google Scholar 

  • Lottermoser BG, Ashley PM, Munksgaard NC (2008) Biogeochemistry of Pb–Zn gossans, northwest Queensland, Australia: implications for mineral exploration and mine site rehabilitation. Appl Geochem 23:723–742

    Article  CAS  Google Scholar 

  • Lu H, Li Z, Fu S, Mendez A, Gasco G, Paz-Ferreiro J (2014) Can biochar and phytoextractors be jointly used for cadmium remediation? PLoS One 9, e95218

    Article  Google Scholar 

  • Moffat AS (1995) Plants proving their worth in toxic metal cleanup. Science 269:302–303

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Novo LAB, Covelo EF, Gonzalez L (2014) Effect of salinity on zinc uptake by Brassica Juncea. Int J Phytoremed 16:704–718

    Article  CAS  Google Scholar 

  • Oomen RJFJ, Wu J, Lelievre F, Blanchet S, Richaud P, Barbier-Brygoo H, Aarts MGM, Thomine S (2009) Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol 181:637–650

    Article  CAS  Google Scholar 

  • Papazoglou EG (2011) Responses of Cynara cardunculus L to single and combined cadmium and nickel treatment conditions. Ecotoxicol Environ Saf 74:195–202

    Article  CAS  Google Scholar 

  • Patra J, Lenka M, Panda BB (1994) Tolerance and co-tolerance of the grass Chloris barbata Sw. to mercury, cadmium and zinc. New Phytol 128:165–171

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Prasad MNV, Sajwan KS, Naidu R (2006) Trace elements in the environment: biogeochemistry, biotechnology, and bioremediation. Taylor & Francis Group, LLC

  • Quartacci MF, Argilla A, Baker AJ, Navari-Izzo F (2006) Phytoextraction of metals from a multiply contaminated soil by Indian mustard. Chemosphere 63:918–925

    Article  CAS  Google Scholar 

  • Rivetta A, Negrini N, Cocucci M (1997) Involvement of Ca2+-calmodulin in Cd2+ toxicity during the early phases of radish (Raphanus sativus L) seed germination. Plant Cell Environ 20:600–608

    Article  CAS  Google Scholar 

  • Salt DE, Blaylock M, Kumar NP, Dushenkov V, Ensley BD, Chet I, Raskin I (1995a) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnology (N Y) 13:468–474

    Article  CAS  Google Scholar 

  • Salt DE, Prince RC, Pickering IJ, Raskin I (1995b) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433

    CAS  Google Scholar 

  • Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167

    Article  CAS  Google Scholar 

  • Schat H, Vooijs RIET (1997) Multiple tolerance and co-tolerance to heavy metals in Silene vulgaris a co-segregation analysis. New Phytol 136:489–496

    Article  CAS  Google Scholar 

  • Shi G, Cai Q (2009) Cadmium tolerance and accumulation in eight potential energy crops. Biotechnol Adv 27:555–561

    Article  CAS  Google Scholar 

  • Singh S, Ramachandran V, Eapen S (2010) Copper tolerance and response of antioxidative enzymes in axenically grown Brassica juncea (L.) plants. Ecotoxicol Environ Saf 73:1975–1981

    Article  CAS  Google Scholar 

  • Tang YT, Qiu RL, Zeng XW, Ying RR, Yu FM, Zhou XY (2009) Lead, zinc, cadmium hyperaccumulation and growth stimulation in Arabis paniculata Franch. Environ Exp Bot 66:126–134

    Article  CAS  Google Scholar 

  • Thomine S, Wang RC, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci U S A 97:4991–4996

    Article  CAS  Google Scholar 

  • Uren NC (1992) Forms, reactions, and availability of nickel in soils. Adv Agron 48:141–203

    Article  CAS  Google Scholar 

  • White PJ, Brown PH (2010) Plant nutrition for sustainable development and global health. Ann Bot 105:1073–1080

    Article  CAS  Google Scholar 

  • Wu LH, Liu YJ, Zhou SB, Guo FG, Bi D, Guo XH, Baker AJM, Smith JAC, Luo YM (2012) Sedum plumbizincicola X.H. Guo et S.B. Zhou ex L.H. Wu (Crassulaceae): a new species from Zhejiang Province, China. Plant Syst Evol 299:487–498

    Article  Google Scholar 

  • Yang XE, Long XX, Ye HB, He ZL, Calvert DV, Stoffella PJ (2004) Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259:181–189

    Article  CAS  Google Scholar 

  • Yoon J, Cao XD, Zhou QX, Ma LQ (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464

    Article  CAS  Google Scholar 

  • Zhao FJ, Lombi E, Breedon T, McGrath SP (2000) Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ 23:507–514

    Article  CAS  Google Scholar 

  • Zornoza P, Sanchez-Pardo B, Carpena RO (2010) Interaction and accumulation of manganese and cadmium in the manganese accumulator Lupinus albus. J Plant Physiol 167:1027–1032

    Article  CAS  Google Scholar 

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Acknowledgments

We thank the Royal Botanic Gardens Victoria for supplying Sedum species, Dr. Trevor Edwards for the identification of plant species, and Mr. Rob Evans for assistance in the experiment. We also thank two anonymous reviewers for constructive comments. This research was supported by the Australian Research Council Linkage Grant LP100100800.

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Authors and Affiliations

  1. Centre for AgriBioscience, La Trobe University, Melbourne Campus, Bundoora, VIC, 3086, Australia

    Chengjun Zhang, Peter W. G. Sale, Gary J Clark & Caixian Tang

  2. Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Wuxing Liu

  3. School of Chemistry, University of Melbourne, Parkville, VIC, 3010, Australia

    Augustine I. Doronila & Spas D. Kolev

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  1. Chengjun Zhang
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  2. Peter W. G. Sale
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Correspondence to Caixian Tang.

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Zhang, C., Sale, P.W.G., Clark, G.J. et al. Succulent species differ substantially in their tolerance and phytoextraction potential when grown in the presence of Cd, Cr, Cu, Mn, Ni, Pb, and Zn. Environ Sci Pollut Res 22, 18824–18838 (2015). https://doi.org/10.1007/s11356-015-5046-x

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