Abstract
This study aimed at determining the cadmium phytoextraction potential of three Populus alba L. clones cultivated in the presence of increasing sodium chloride concentrations. Plantlets of a commercial and two autochthonous poplar clones were grown in perlite with nutrient solution enriched in CdSO4 (50 and 100 μM) and NaCl (25 and 50 mM), administered either alone or in combination. The three clones showed significant variation not only in cadmium and salt tolerance, accumulation and content, but also in the effect of the interaction between the two elements on these parameters. The toxic effect of Cd and salt excess on plants was mutually exacerbated by the presence of both. Even though the outcome of the joint treatment was always a decrease in shoot Cd or Na accumulation, the three clones showed variation in the extent of such reduction. Evaluating the total element content per plant shoot, the fast-growing commercial clone displayed the highest phytoextraction potential for Cd and Na, either alone or in mixture. Our results demonstrated for the first time that the Cd response in presence of salt can vary in the different clones.
Similar content being viewed by others
References
Acosta JA, Jansen B, Kalbitz K, Faz A, Martínez-Martínez S (2011) Salinity increases mobility of heavy metals in soils. Chemosphere 85:1318–1324. https://doi.org/10.1016/j.chemosphere.2011.07.046
Ahmad A, Hadi F, Ali N (2015) Effective phytoextraction of cadmium (Cd) with increasing concentration of total phenolics and free proline in Cannabis sativa (L.) plant under various treatments of fertilizers, plant growth regulators and sodium salt. Int J Phytoremediat 17:56–65. https://doi.org/10.1080/15226514.2013.828018
Ali H, Khan E, Ilahi I (2019) Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J Chem-NY:6730305. https://doi.org/10.1155/2019/6730305
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. Ecotox Environ Safe 85:13–22. https://doi.org/10.1016/j.ecoenv.2012.08.019
Beritognolo I, Piazzai M, Benucci S, Kuzminsky E, Sabatti M, Scarascia Mugnozza G, Muleo R (2007) Functional characterization of three Italian Populus alba L. genotypes under salinity stress. Trees 21:465–477. https://doi.org/10.1007/s00468-007-0139-x
Bettarini I, Colzi I, Coppi A, Falsini S, Echevarria G, Pazzagli L, Selvi F, Gonnelli C (2019) Unravelling soil and plant metal relationships in Albanian nickel hyperaccumulators in the genus Odontarrhena (syn. Alyssum sect. Odontarrhena, Brassicaceae). Plant Soil 440:135–149. https://doi.org/10.1007/s11104-019-04077-y
Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohyd Res 344:1879–1900. https://doi.org/10.1016/j.carres.2009.05.021
Capuana M, Colzi I, Buccianti A, Coppi A, Palm E, Del Bubba M, Gonnelli C (2018) Paradoxical effects of density on measurement of copper tolerance in Silene paradoxa L. Environ Sci Pollut Res 25:1331–1339. https://doi.org/10.1007/s11356-017-0593-y
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. S Afr J Bot 85:63–69. https://doi.org/10.1016/j.sajb.2012.12.004
Chen S, Li J, Fritz E, Wang S, Hüttermann A (2002) Sodium and chloride distribution in roots and transport in three poplar genotypes under increasing NaCl stress. Forest Ecol Manag 168:217–230. https://doi.org/10.1016/S0378-1127(01)00743-5
Cheng M, Kopittke PM, Wang A, Tang C (2019) Salinity decreases Cd translocation by altering Cd speciation in the halophytic Cd-accumulator Carpobrotus rossii. Ann Bot-London 123:121–132. https://doi.org/10.1093/aob/mcy148
Colzi I, Doumett S, Del Bubba N, Fornaini J, Arnetoli M, Gabbrielli R, Gonnelli C (2011) On the role of the cell wall in the phenomenon of copper tolerance in Silene paradoxa L. Environ Exp Bot 72:77–83. https://doi.org/10.1016/j.envexpbot.2010.02.006
Colzi I, Lastrucci L, Rangoni M, Coppi A, Gonnelli C (2018) Using Myriophyllum aquaticum (Vell.) Verdc. to remove heavy metals from contaminated water: better dead or alive? J Environ Manag 213:320–328. https://doi.org/10.1016/j.envexpbot.2010.02.006
Confalonieri M, Balestrazzi A, Bisoffi S, Carbonera D (2003) In vitro culture and genetic engineering of Populus spp.: synergy for forest tree improvement. Plant Cell Tiss Org 72:109–138. https://link.springer.com/article/10.1023/A:1022265504775
Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379. https://doi.org/10.1016/j.tplants.2014.02.001
Dermont G, Bergeron M, Mercier G, Richer-Lafleche M (2008) Soil washing for metal removal: a review of physical/chemical technologies and field applications. J Hazard Mater 152:1–31. https://doi.org/10.1016/j.jhazmat.2007.10.043
Di Lonardo S, Capuana M, Arnetoli M, Gabbrielli R, Gonnelli C (2011) Exploring the metal phytoremediation potential of three Populus alba L. clones using an in vitro screening. Environ Sci Pollut Res 18:82–90. https://doi.org/10.1007/s11356-010-0354-7
Ghallab A, Usman ARA (2007) Effect of sodium chloride-induced salinity on phyto-availability and speciation of Cd in soil solution. Water Air Soil Pollut 185:43–51. https://doi.org/10.1007/s11270-007-9424-y
Ghnaya T, Slama I, Messedi D, Grignon C, Ghorbel MH, Abdelly C (2007) Cd-induced growth reduction in the halophyte Sesevium portulacastrum is significantly improved by NaCl. J Plant Res 120:309–316. https://doi.org/10.1007/s10265-006-0042-3
Grignon C, Sentenac H (1991) pH and ionic conditions in the apoplast. Ann Rev. Plant Physiol 42:103–128. https://www.annualreviews.org/doi/pdf/10.1146/annurev.pp.42.060191.000535
Han RM, Lefèvre 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. https://doi.org/10.1007/s10725-012-9697-z
He J, Ma C, Ma Y, Li H, Kang J, Liu T, Polle A, Peng C, Luo ZB (2013) Cadmium tolerance in six poplar species. Environ Sci Pollut Res 20:163–174. https://doi.org/10.1007/s11356-012-1008-8
Houda Z, Bejaoui Z, Albouchi A, Gupta DK, Corpas FJ (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). Environ Monit Assess 188:99. https://doi.org/10.1007/s10661-016-5102-0
Hu Y, Nan Z, Su J, Wang N (2013) Heavy metal accumulation by poplar in calcareous soil with various degrees of multi-metal contamination: implications for phytoextraction and phytostabilization. Environ Sci Pollut Res 20:7194–7203. https://doi.org/10.1007/s11356-013-1711-0
IARC (International Agency for Research on Cancer) (2016) IARC monographs on the evaluation of carcinogenic risks to humans. Volumes 1–115
Ismael MA, Elyamine AM, Moussa MG, Cai M, Zhao X, Hu C (2019) Cadmium in plants: uptake, toxicity, and its interactions with selenium fertilizers. Metallomics 11:255–277. https://doi.org/10.1039/C8MT00247A
Krzesłowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51. https://doi.org/10.1007/s11738-010-0581-z
Kumar M, Gogoi A, Kumari D, Borah R, Das P, Mazumder P, Kumar Tyagi V (2017) Review of perspective, problems, challenges, and future scenario of metal contamination in the urban environment. J Hazard Toxic Radioact Waste 21:04017007. https://ascelibrary.org/doi/pdf/10.1061/%28ASCE%29HZ.2153-5515.0000351
Lutts S, Lefèvre I (2015) How can we take advantage of halophyte properties to cope with heavy metal toxicity in salt-affected areas? Ann Bot-London 115:509–528. https://doi.org/10.1093/aob/mcu264
Mahar A, Wang P, Ali A, Awasthi MK, Lahori AH, Wang Q, Li R, Zhang Z (2016) Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: a review. Ecotox Environ Safe 126:111–121. https://doi.org/10.1016/j.ecoenv.2015.12.023
Mani D, Kumar C (2014) Biotechnological advances in bioremediation of heavy metals contaminated ecosystems: an overview with special reference to phytoremediation. Int J Environ Sci Technol 11:843–872. https://doi.org/10.1007/s13762-013-0299-8
McLaughlin MJ, Palmer LT, Tiller KG, Beech TA, Smart MK (1994) Increased soil salinity causes elevated cadmium concentrations in field grown potato tubers. J Environ Qual 23:1013–1018. https://doi.org/10.2134/jeq1994.00472425002300050023x
Mei XQ, Li SS, Li QS, Yang YF, Luo X, He BY, Li H, Xu ZM (2014) Sodium chloride salinity reduces Cd uptake by edible amaranth (Amaranthus mangostanus L.) via competition for Ca channels. Ecotox Environ Safe 105:59–64. https://doi.org/10.1016/j.ecoenv.2014.04.005
Nikolić N, Zorić L, Cvetković I, Pajević S, Borišev M, Orlović S, Pilipović A (2017) Assessment of cadmium tolerance and phytoextraction ability in young Populus deltoides L. and Populus × euramericana plants through morpho-anatomical and physiological responses to growth in cadmium enriched soil. iForest 10:635–644. https://doi.org/10.3832/ifor2165-010
Novo LAB, Manousaki E, Kalogerakis N, González L (2014) The effect of cadmium and salinity on germination and early growth of Brassica juncea (L.) var. juncea. Fresenius Environ Bull 22:3709–3717
Panta S, Flowers T, Lane P, Doyle R, Haros G, Shabala S (2014) Halophyte agriculture: success stories. Environ Exp Bot 107:71–83. https://doi.org/10.1016/j.envexpbot.2014.05.006
Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut Res 22:4056–4075. https://doi.org/10.1007/s11356-014-3739-1
Pelloux J, Rusterucci C, Mellerowicz EJ (2007) New insight into pectin methylesterase structure and function. Trends Plant Sci 12:267–277. https://doi.org/10.1016/j.tplants.2007.04.001
Pignattelli S, Colzi I, Buccianti A, Cecchi L, Arnetoli M, Monnanni R, Gabbrielli R, Gonnelli C (2012) Exploring element accumulation patterns of a metalexcluder plant naturally colonizing a highly contaminated soil. J Hazard Mater 227:362–369
Pitman MG, Läuchli A (2002) Global impact of salinity and agricultural ecosystems. In: Läuchli A, Lüttge U (eds) Salinity: environment – plants - molecules. Springer, Dordrecht, pp 3–20. https://link.springer.com/chapter/10.1007/0-306-48155-3_1
Rafati-Rahimzadeh M, Rafati-Rahimzadeh M, Kazemi S, Moghadamnia A (2017) Cadmium toxicity and treatment: an update. Caspian J Intern Med 8:135–145. https://doi.org/10.22088/Fcjim.8.3.135
Robinson BH, Mills TM, Petit D, Fung LE, Green SR, Clothier BE (2000) Natural and induced cadmium-accumulation in poplar and willow: implications for phytoremediation. Plant Soil 227:301–306. https://doi.org/10.1023/A:1026515007319
Ruttens A, Boulet J, Weyens N, Smeets K, Adriaensen K, Meers E, van Slycken S, Tack F, Meiresonne L, Thewys T, Witters N, Carleer R, Dupae J, Vangronsveld J (2011) Short rotation coppice culture of willows and poplars as energy crops on metal contaminated agricultural soils. Int J Phytoremediat 13:194–207. https://doi.org/10.1080/15226514.2011.568543
Shafi M, Bakht J, Hassan MJ, Raziuddin M, Zhang GP (2009) Effect of cadmium and salinity stresses on growth and antioxidant enzyme activities of wheat (Triticum aestivum L.). B Environ Contam Tox 82:772–776. https://doi.org/10.1007/s00128-009-9707-7
Smolders E, Mertens J (2012) Cadmium. In: Alloway BJ (ed) Heavy metals in soils. Springer, Dordrecht, pp 283–311
Thijs S, Witters N, Janssen J, Ruttens A, Weyens N, Herzig R, Mench M, van Slycken S, Meers E, Meiresonne L, Vangronsveld J (2018) Tobacco, sunflower and high biomass SRC clones show potential for trace metal phytoextraction on a moderately contaminated field site in Belgium. Front Plant Sci 9:1879. https://doi.org/10.3389/fpls.2018.01879
Tognetti R, Cocozza C, Marchetti M (2013) Shaping the multifunctional tree: the use of Salicaceae in environmental restoration. iForest 6:37–47. https://doi.org/10.3832/ifor0920-006
Tudoreanu L, Philips CJC (2004) Empirical models of cadmium accumulation in maize, rye grass and soya bean plants. J Sci Food Agr 84:845–852
US Environmental Protection Agency (EAT) (2000) Introduction of toxic metals. EPA/600/R-99/107. Cincinnati, OH: National Risk Management Research Laboratory, Office of Research and Development
Usman ARA, Kuzyakov Y, Stahr K (2005) Effect of immobilizing substances and salinity on heavy metals availability to wheat grown on sewage sludge-contaminated soil. Soil Sediment Contam 14:329–344. https://doi.org/10.1080/15320380590954051
Van Oosten J, Maggio A (2015) Functional biology of halophytes in the phytoremediation of heavy metal contaminated soils. Environ Exp Bot 111:135–146. https://doi.org/10.1016/j.envexpbot.2014.11.010
Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794. https://doi.org/10.1007/s11356-009-0213-6
Weggler K, McLaughlin MJ, Graham RD (2004) Effect of chloride in soil solution on the plant availability of biosolid-borne cadmium. J Environ Qual 33:496–504. https://doi.org/10.2134/jeq2004.4960
Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. Int Sch Res Network ISRN Ecol:1–20. https://doi.org/10.5402/2011/402647
Zalesny RS Jr, Bauer EO (2007) Evaluation of Populus and Salix continuously irrigated with landfill leachate I. Genotype-specific elemental phytoremediation. Int J Phytoremediat 9:281–306. https://doi.org/10.1080/15226510701476461
Zalesny JA, Zalesny RS Jr, Wiese AH, Sexton B, Hall RB (2008) Sodium and chloride accumulation in leaf, woody, and root tissue of Populus after irrigation with landfill leachate. Environ Pollut 155:72-80. https://doi.org/10.1016/j.envpol.2007.10.032
Acknowledgments
Mrs. Catia Boggi (IBBR-CNR) is gratefully acknowledged for her precious technical support.
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Elena Maestri
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Capuana, M., Bianchi, E., Cencetti, G. et al. Extracting cadmium in the presence of salt: a study on three poplar clones under controlled conditions. Environ Sci Pollut Res 28, 1040–1051 (2021). https://doi.org/10.1007/s11356-020-10536-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-10536-2