BACKGROUND: Many areas throughout the world are simultaneously contaminated by high concentrations of soluble salts and by high concentrations of heavy metals that constitute a serious threat to human health. The use of plants to extract or stabilize pollutants is an interesting alternative to classical expensive decontamination procedures. However, suitable plant species still need to be identified for reclamation of substrates presenting a high electrical conductivity. SCOPE: Halophytic plant species are able to cope with several abiotic constraints occurring simultaneously in their natural environment. This review considers their putative interest for remediation of polluted soil in relation to their ability to sequester absorbed toxic ions in trichomes or vacuoles, to perform efficient osmotic adjustment and to limit the deleterious impact of oxidative stress. These physiological adaptations are considered in relation to the impact of salt on heavy metal bioavailabilty in two types of ecosystem: (1) salt marshes and mangroves, and (2) mine tailings in semi-arid areas. CONCLUSIONS: Numerous halophytes exhibit a high level of heavy metal accumulation and external NaCl may directly influence heavy metal speciation and absorption rate. Maintenance of biomass production and plant water status makes some halophytes promising candidates for further management of heavy-metal-polluted areas in both saline and non-saline environments.

Groupe de Recherche en Physiologie végétale Place Croix du Sud 1348 Louvain la Neuve France and Institute of Plant Molecular Biology Biology Centre CAS Branišovská 31 37005 České Budějovice Czech Republic

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Acosta JA, Jansen B, Kalbitz K, Faz A, Martínez-Martínez S. 2011. Salinity increases mobility of heavy metals in soils. Chemosphere 85: 1318–1324. PubMed

Adrian-Romero MS, Wilson J, Blunden G, Yang MH, Carabot-Cuervo A, Bashir AK. 1998. Betaines in coastal plants. Biochemical Systematics and Ecology 26: 535–543.

Agoramoorthy G, Chen FA, Hsu MJ. 2008. Threat of heavy metal pollution in halophytic and mangrove plants of Tamil Nadu, India. Environmental Pollution 155: 320–326. PubMed

Agarie S, Shimoda T, Shimizu Y, et al. 2007. Salt tolerance, salt accumulation, and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant PubMed

Badi HN, Sorooshzadeh A. 2011. Evaluating potential of borage (

Baker AJM, Brooks RR. 1989. Terrestrial higher plants which hyperaccumulate metallic elements – a review of their distribution, ecology and phytochemistry. Biorecovery 1: 81–126.

Barceló J, Poschenrieder C. 1990. Plant water relations as affected by heavy metal stress: a review. Journal of Plant Nutrition 13: 1–37.

Barceló J, Poschenrieder C. 2003. Phytoremediation: principles and perspectives. Contribution to Science 2: 333–344.

Barceló J, Vásquez MD, Poschenrieder C. 1988. Cadmium-induced structural and ultrastructural changes in the vascular system of bush bean stems. Botanica Acta 101: 254–261.

Batty LC, Dolan C. 2013. The potential use of phytoremediation for sites with mixed organic and inorganic contamination. Critical Reviews in Environmental Science and Technology 43: 217–259.

Ben Rejeb K, Ghanya T, Zaier H, et al. 2013. Evaluation of the Cd

Bertin C, Yang X, Weston LA. 2003. The role of root exudates and allelochemicals in the rhizosphere. Plant and Soil 256: 67–83.

Bingham FT, Strong JE, Sposito G. 1983. Influence of chloride salinity on cadmium uptake by Swiss chard. Soil Science 135: 160–165.

Bingham FT, Sposito G, Strong JE. 1984. The effect of chloride on the availability of cadmium. Journal of Environmental Quality 13: 71–74.

Bingham FT, Sposito G, Strong JE. 1986. The effect of sulfate on the availability of cadmium. Soil Science 141: 172–177.

Bose J, Rodrigo-Moreno A, Shabala S. 2014. ROS homeostasis in halophytes in the context of salinity tolerance. Journal of Experimental Botany 65: 1241–1257. PubMed

Boularbah A, Morel JL, Bitton G, Mench M. 1996. A direct solid-phase assay specific for heavy-metal toxicity. II. Assessment of heavy-metal immobilization in soils and bioavailability to plants. Soil and Sediment Contamination 5: 395–404.

Briat JF, Lobréaux S. 1997. Iron transport and storage in plants

Burke DJ, Weis JS, Weis P. 2000. Release of metals by the leaves of the salt marsh grasses

Caçador I, Vale C, Catarino F. 2000. Seasonal variation of Zn, Pb, Cu and Cd concentrations in the root-sediment system of PubMed

Caçador I, Caetano M, Duarte B, Vale C. 2009. Stock and losses of trace metals from salt marsh plants. Marine Environmental Research 67: 75–82. PubMed

Caetano M, Vale C, Cesario R, Fonseca N. 2008. Evidence for preferential depths of metal retention in roots of salt marsh plants. Science of the Total Environment 390: 466–474. PubMed

Cambrollé J, Redondo-Gómez S, Mateos-Naranjo E, Figueroa ME. 2008. Comparison of the role of two PubMed

Cambrollé J, Mancilla-Leytón JM, Muñoz-Vallés S, Luque T, Figueroa ME. 2012. Zinc tolerance and accumulation in the salt-marsh shrub PubMed

Cambrollé J, Mateos-Naranjo E, Redondo-Gómez S, Luque T, Figueroa ME. 2011. The role of two

Caravaca F, Del Mar Alguacil M, Torres P, Roldán A. 2005. Microbial activities and arbuscular mycorrhizal fungi colonization in the rhizosphere of the salt marsh plant

Carbonell-Barrachina MA, Aarabi MA, DeLaune RD, Gambrell RP, Patrick WH., Jr 1998. The influence of arsenic chemical form and concentration on

Carrasco L, Caravaca F, Alvarez-Rogel J, Roldán A. 2006. Microbial processes in the rhizosphere soil of a heavy metals-contaminated Mediterranean salt marsh: a facilitating role of AM fungi. Chemosphere 64: 104–111. PubMed

Carrier P, Baryla A, Havaux M. 2003. Cadmium distribution and microlocalization in oilseed rape ( PubMed

Carvalho SM, Caçador I, Martins-Loução MA. 2006. Arbuscular mycorrhizal fungi enhance root cadmium and copper accumulation in the roots of the salt marsh plant

Castro R, Pereira S, Lima A, et al. 2009. Accumulation, distribution and cellular partitionning of mercury in several halophytes of a contaminated salt marsh. Chemosphere 76: 1348–1355. PubMed

Chaignon V, Di Malta D, Hinsinger P. 2002. Fe-deficiency increases Cu acquisition by wheat cropped in a Cu-contaminated vineyard soil. New Phytologist 154: 121–130.

Chaturvedi AK, Mishra A, Tiwari V, Jha B. 2012. Cloning and transcript analysis of type 2 metallothionein gene ( PubMed

Chaudhri II, Shah BH, Naqvi N, Mallick IA. 1964. Investigations on the role of

Choi YE, Harada E, Kim GH, Yoon ES, Sano H. 2004. Distribution of elements on tobacco trichomes and leaves under cadmium and sodium stresses. Journal of Plant Biology 47: 75–82.

Choi YE, Harada E, Wada M, et al. 2001. Detoxification of cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta 213: 45–50. PubMed

Cobbett C. 2003. Heavy metals and plants – model systems and hyperacculmulators. New Phytologist 159: 289–293. PubMed

Cobbett C, Goldsbrough PB. 2002. Phytochelatins and metallothionein: roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology 53: 159–182. PubMed

Colmer TD, Flowers TJ. 2008. Flooding tolerance in halophytes. New Phytologist 179: 964–974. PubMed

Conesa HM, Evangelou MWH, Robinson BH, Schulin R. 2012. A critrical review of current state of phytotechnologies to remediate soils: still a promising tool? Scientific World Journal 2012. PubMed PMC

Cong M, Lv J, Liu X, Zhao J, Wu H. 2013. Gene expression responses in PubMed PMC

D’Amore JJ, Al-Abed SR, Schekel KG, Ryan JA. 2005. Methods for speciation of metals in soils: a review. Journal of Environmental Quality 34: 1707–1745. PubMed

Degryse F, Smolders E, Merckx R. 2006. Labile Cd complexes increase Cd availability to plants. Environmental Science and Technology 40: 830–836. PubMed

de la Rosa G, Peralta-Videa JR, Montes M, Parsons JG, Cano-Aguilera I, Gardea-Torresdey JL. 2004. Cadmium uptake and translocation in tumbleweed ( PubMed

Demidchik V. 2014. Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Journal of Experimental Botany 109: 212–228.

Demidchik V, Cuin TA, Svistunenko D, et al. 2010. PubMed

De Vos AC, Broekman R, de Almeida Guerra CC, van Rijsselberghe M, Rozema J. 2013. Developing and testing new halophyte crops: A case study of salt tolerance of two species of the Brassicaceae,

Doyle MO, Otte ML. 1997. Organism-induced accumulation of iron, zinc and arsenic in wetland soils. Environmental Pollution 96: 1–11. PubMed

Drazkiewicz M, Baszyńki T. 2005. Growth parameters and photosynthetic pigments in leaf segments of PubMed

Duarte B, Delgado M, Caçador I. 2007. The role of citric acid in cadmium and nickel uptake and translocation in PubMed

Duarte B, Reboreda R, Caçador I. 2008. Seasonal variation of extracellular enzymatic activity (EEA) and its influence on metal speciation in a polluted salt marsh. Chemosphere 73: 1056–1063. PubMed

Eid MA. 2011. Halophytic plants for phytoremediation of heavy metals contaminated soil. Journal of American Science 7: 377–382.

Eisa SS, Eid MA. 2011. Assessment of the phytoextraction potential of some fast growing halophytes and maize plants. Australian Journal of Basic and Applied Science 5: 88–95.

Ernst WHO, Nelissen HJM. 2000. Life-cycle phases of a zinc- and cadmium-resistant ecotype of PubMed

European Environment Agency. 2007. Progress in management of contaminated sites (CSI015)

Flowers TJ, Colmer TD. 2008. Salinity tolerance in halophytes. New Phytologist 179: 945–96. PubMed

Flowers TJ, Galal HK, Bromham L. 2010. Evolution of halophytes: multiple origins of salt tolerance in land plants. Functional Plant Biology 37: 604–612.

Fox DI, Pichler T, Yeh DH, Alcantar NA. 2012. Removing heavy metal in water: the interactions of cactus mucilage and arsenate (As(V)). Environmental Science and Technology 46: 4553–4559. PubMed

Garcia-Miragaya J, Page AL. 1976. Influence of ionic strength and inorganic complex formation on the sorption of trace amounts of Cd by Montmorillonite. Soil Science Society of America Journal 40: 658–663.

Ghanem ME, Han RM, Classen B, et al. 2010. Mucilage and polysaccharides in the halophyte plant species PubMed

Ghnaya T, Slama I, Messedi D, Grignon C, Ghorbel MH, Abdelly C. 2007a. Effects of Cd PubMed

Ghnaya T, Slama I, Messedi D, Grignon C, Ghorbel MH, Abdelly C. 2007b. Cd-induced growth reduction in the halophyte PubMed

Ghnaya T, Nouairi I, Slama I, et al. 2005. Cadmium effects on growth and mineral nutrition of two halophytes: PubMed

Ghnaya T, Zaier H, Baioui R, et al. 2013. Implications of organic acids in the long-distance transport and accumulation of lead in PubMed

Ghelis T, Dellis O, Jeannette E, Bardat F, Miginiac E, Sotta B. 2000. Abscisic acid plasmalemma perception triggers a calcium influx essential for RAB18 gene expression in PubMed

Girault L, Boudou A, Dufourc EJ. 1998. PubMed

Gorai M, El Aloui W, Yang X, Neffati M. 2014. Towards understanding the ecological role of mucilage in seed germination of a desert shrub

Greger M, Ögren E. 1991. Direct and indirect effects of Cd

Gonzalez-Mendoza D, Moreno AQ, Zapata-Perez O. 2007. Coordinated responses of phytochelatin synthase and metallothionein genes in black mangrove, PubMed

Göhre V, Paszkowski U. 2006. Contribution of the abuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223: 1115–1122. PubMed

Guo Y, Bundithya W, Goldsbrough PB. 2003. Characterization of the metallothionein gene family: tissue-specific expression and induction during senescence and in response to copper. New Phytologist 159: 369–381. PubMed

Gutknecht J. 1981. Inorganic mercury (Hg

Han RM, Lefèvre I, Ruan CJ, Qin P, Lutts S. 2012a. NaCl differently interferes with Cd and Zn toxicities in the wetland halophyte species

Han RM, Lefèvre I, Ruan CJ, Beukelaers N, Qin P, Lutts S. 2012b. Effects of salinity on the response of the wetland halophyte

Han RM, Lefèvre I, Albacete A, et al. 2013a. Antioxidant enzyme activities and hormonal status in response to Cd stress in wetland halophyte PubMed

Han RM, Quinet M, André E, et al. 2013b. Accumulation and distribution of Zn in the shoots and reproductive structures of the halophyte plant species PubMed

Hatje V, Payne TE, Hill DM, McOrist G, Birch GF, Szymczak R. 2003. Kinetics of trace element uptake and release by particles in estuarine waters: effects of pH, salinity, and particle loading. Environment International 29: 619–629. PubMed

Helal HM, Upenov A, Issa GJ. 1999. Growth and uptajke of Cd and Zn by

Hempel M, Botté SE, Negrin VL, Chiarello MN, Marcovecchio JE. 2008. The role of the smooth cordgrass

Hernandez-Soriano MC, Degryse F, Lombi E, Smolders E. 2012. Mangenese toxicity in barley is controlled by solution manganese and soil manganese speciation. Soil Science Society of America Journal 76: 399–407.

Hildebrandt U, Regvar M, Bothe H. 2007. Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68: 139–146. PubMed

Huang GY, Wang YS. 2009. Expression analysis of type 2 metallothionein gene in mangrove species ( PubMed

Huang GY, Wang YS. 2010. Expression and characterization analysis of type 2 metallothiobnein from grey mangrove species ( PubMed

Jackson WA, Pardue JH. 1999. Potential for enhancement of biodegradation of crude oil in Louisiana salt marshes using nutrient amendments. Water Air and Soil Pollution 109: 343–355.

Javed MT, Stoltz E, Lindberg S., Greger M. 2013. Changes in pH and organic acids in mucilage of PubMed

Jithesh MN, Prashanth SR, Sivaprakash KR, Parida AK. 2006a. Monitoring expression profiles of antioxidant genes to salinity, iron, oxidative, light and hyperosmotic stresses in the highly salt tolerant grey mangrove, PubMed

Jithesh MN, Prashanth SR, Sivaprakash KR, Parida AK. 2006b. Antioxidative response mechnisms in halophytes: their role in stress defence. Journal of Genetics 85: 237–254. PubMed

Jordan FL, Robin-Abbott M, Maier RM, Glenn EP. 2002. A comparison of chelator-facilitated metal uptake by a halophyte and a glycophyte. Environmental Toxicology and Chemistry 21: 2698–2704. PubMed

Kadukova J, Kalogerakis N. 2007. Lead accumulation from non-saline and saline environment by

Katschnig D, Broekman R, Rozema J. 2013. Salt tolerance in the halophyte

Kiyono M, Oka Y, Sone Y, et al. 2012. Expression of the bacterial heavy metal transporter MerC fused with a plant SNARE, SYP121, in PubMed

Koren Š, Arčon I, Kump P, Nečemer M, Vogel-Mikuš K. 2013. Influence of CdCl

Kumpiene J, Lagerkvist A, Maurice C. 2008. Stabilization of As, Cr, Cu, Pb and Zn in soil using amendments – A review. Waste Management 28: 215–225. PubMed

Laffont-Schwob I, d’Enjoy-Weinkammerer G, Pricop A, Prudent P, Masotti V, Rabier J. 2011. Evalutation of a potential candidate for heavy metal phytostabilization in polluted sites of the Mediterranean littoral (SE Marseille): endomycorrhizal status, fitness biomarkers and metal content of

Lakshmanraj L, Gurusamy A, Gobinath MB, Chandramohan R. 2009. Studies on biosorption of hexavalent chromium from aqueous solutions by using boiled mucilaginous seeds of PubMed

Lefèvre I. 2007. Investigation of three Mediterranean plant species suspected to accumulate and tolerate high cadmium and zinc levels. PhD Thesis, Université catholique de Louvain, Louvain-la-Neuve, Belgium.

Lefèvre I, Correal E, Lutts S. 2005. Cadmium tolerance and accumulation in the noxious weed

Lefèvre I, Correal E, Faz-Cano Á, Zanuzzi A, Lutts S. 2009a. Structural development, water status, pigment concentrations, and oxidative stress of

Lefèvre I, Marchal G, Meerts P, Corréal E, Lutts S. 2009b. Chloride salinity reduces cadmium accumulation by the Mediterranean halophyte species

Lefèvre I, Correal E, Lutts S. 2010a. Impact of cadmium and zinc on growth and water status of PubMed

Lefèvre I, Marchal G, Ghanem ME, Correal E, Lutts S. 2010b. Cadmium has contrasting effects on polyethylene glycol – sensitive and resistant cell lines in the Mediterranean halophyte species PubMed

Lefèvre I, Vogel-Mikuš K, Jeromel L, et al. 2014. Differential cadmium and zinc distribution in relation to their physiological impact in the leaves of the accumulating PubMed

Li YM, Chaney RL, Schneiter AA. 1994. Effect of soil chloride level on cadmium concentration in sunflower kernels. Plant and Soil 167: 275–280.

Li L, Liu X, Peijnenburg WJGM, et al. 2012. Pathways of cadmium fluxes in the root of the halophyte PubMed

Liao JP, Lin XG, Cao ZH, Shi YQ, Wong MH. 2003. Interactions between arbuscular mycorrhizae and heavy metals under sand culture experiment. Chemosphere 50: 847–853. PubMed

Liu X, Yang C, Zhang L, et al. 2011. Metabolic profiling of cadmium-induced effects in one pioneer intertidal halophyte PubMed

Lokhande VH, Gor BK, Desai NS, Nikam TD, Suprasanna P. 2013.

Lokhande VH, Srivastava S, Patade VY, et al. 2011. Investigation of arsenic accumulation and tolerance in PubMed

Lombi E, Wenzel WW, Gobran GR, Adriano DC. 2001. Dependency of phytoavailability of metals on indigenous and induced rhizosphere processes: a review. In: Gobran GR, Wenzel WW, Lombi E, eds. Trace elements in the rhizosphere. Boca Raton, FL: CRC Press, 3–24.

Lutts S, Hausman JF, Quinet M, Lefèvre I. 2013. Polyamines and their roles in the alleviation of ion toxicities in plants. In: Ahmad P, Azooz MM, Prasad MNV, eds. Ecophysiology and responses of plants under salt stress. New York: Springer, Science + business media, 315–353.

Lutts S, Lefèvre I, Delpérée C, et al. 2004. Heavy metal accumulation by the halophyte species Mediterranean saltbush. Journal of Environmental Quality 33: 1271–1279. PubMed

Mahon S, Carman KR. 2008. The influence of salinity on the uptake, distribution, and excretion of metals by the smooth cordgrass,

Manousaki E, Kalogerakis N. 2009. Phytoextraction of Pb and Cd by the Mediterranean saltbush ( PubMed

Manousaki E, Kadukova J, Papadantonakis N, Kalogerakis N. 2008. Phytoextraction and phytoexcretion of Cd by the leaves of PubMed

Marschner H. 1995. Mineral nutrition of higher planrts. San Diego: Academic Press.

Mateos-Naranjo E, Redondo-Gómez S, Cambrollé J, Figueroa ME. 2008a. Growth and photosynthetic responses to copper stress of an invasive cordgrass, PubMed

Mateos-Naranjo E, Redondo-Gómez S, Cambrollé J, Luque T, Figueroa ME. 2008b. Growth and photosynthetic responses to zinc stress o fan invasive cordgrass, PubMed

Mazharia M, Homaeed M. 2012. Annual halophyte

McFarlane GR, Burchett M. 1999. Zinc distribution and excretion in leaves of the grey mangrove

McFarlane GR, Burchett M. 2000. Cellular distribution of copper, lead and zinc in the grey mangrove,

McLaughlin MJ, Tiller KG, Beech T, Smart MK. 1994. Soil salinity causes elevated cadmium concentration in field-grown potato tubers. Journal of Environmental Quality 23: 1013–1018. PubMed

Mendez MO, Maier RM. 2008. Phytoremediation of mine tailings in temperate and arid environments. Review of Environmental Science and Biotechnology 7: 47–59.

Mendez MO, Glenn EP, Maier RM. 2007. Phytostabilization potential of quailbush for mine tailings: growth, metal accumulation, and microbial community changes. Journal of Environmental Quality 36: 245–253. PubMed

Migeon A, Blaudez D, Wilkins O, et al. 2010. Genome-wide analysis of plant metal transporters, with an emphasis on poplar. Cellular and Molecular Life Science 67: 3763–3784. PubMed PMC

Migocka M, Papierniak A, Kosatka E, Klobus G. 2011. Comparative study of the active cadmium efflux systems operating at the plasma membrane and tonoplast of cucumber root cells. Journal of Experimental Botany 62: 4903–49012. PubMed PMC

Milić D, Luković J, Ninkov J, et al. 2012. Heavy metal content in halophytic plants from inland and maritime saline areas. Central European Journal of Biology 7: 307–317.

Miyasaka SC, Hawes MC. 2001. Possible role of root border cells in detection and avoidance of aluminium toxicity. Plant Physiology 125: 1978–1987. PubMed PMC

Mohaptra S, Minocha R, Long S, Minocha SC. 2009. Putrescine overproduction negatively impacts the oxidative state of poplar cells in culture. Plant Physiology and Biochemistry 47: 262–271. PubMed

Morel JL, Mench M, Guckert A. 1986. Measurements of Pb

Moreno FN, Anderson CWN, Sytewart RB, Robinson BH. 2005. Mercury volatilization and phytoextraction from base-metal mine tailings. Environmental Pollution 136: 341–352. PubMed

Mucha AP, Almeida CM, Bordalo AA, Vasconcelos MT. 2005. Exudation of organic acids by a marsh plant and implication on trace metal availability in the rhizosphere of estuarine sediments. Estuarine and Coastal Shelf Science 65: 191–198.

Mühlingh KH, Läuchli 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 and Soil 253: 219–231.

Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annual Review of Plant Biology 59: 651–681. PubMed

Nagata T, Morita H, Akizawa T, Pan-Hou H. 2010. Development of a transgenic tobacco plant for phytoremediation of methylmercury pollution. Applied Microbiology Biotechnology 87: 781–786. PubMed

Nečemer M, Kump P, Ščančar J, et al. 2008. Application of X-ray fluorescence analytical techniques in phytoremediation and plant biology studies. Spectrochimica Acta – Part B Atomic Spectroscopy 63: 1240–1247.

Oomen RJ, Wu J, Lelievre F, et al. 2009. Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator PubMed

Otero XL, Macias F. 2002. Variation with depth and season in metal sulfide in salt marsh soils. Biogeochemistry 61: 247–268.

Ozgur R, Uzilday B, Sekmen AH, Turkan I. 2013. Reactive oxygen species regulation and antioxidant defence in halophytes. Functional Plant Biology 40: 832–847. PubMed

Ozkutlu F, Ozturk L, Erdem H, McLaughlin M, Cakmak I. 2007. Leaf-applied sodium chloride promotes cadmium accumulation in durum wheat grain. Plant and Soil 290: 323–331.

Pan X, Yang J, Zhang D, Mu S. 2012. Lead complexation of root exudates of salt marsh plant

Pan X, Yang J, Zhang D, Chen X, Mu S. 2011. Cu(II) complexation of high molecular weight (HMW) fluorescent substances in root exudates from a wetland halophyte ( PubMed

Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C. 2002. Heavy metal toxicity: cadmium penetrates through calcium channels and disturbs the plant water status. Plant Journal 32: 539–548. PubMed

Petraglia A, De Benedictis M, Degoila F, et al. 2014. The capability to synthesize phytochelatins and the presence of constitutive and functional phytochelatin synthases are ancestral (plesiomorphic) characters for basal land plants. Journal of Experimental Botany 65: 1153–1163. PubMed

Pilon-Smits EA, Zhu YL, Sears T, Terry N. 2000. Overexpression of glutathione reductase in

Pongrac P, Vogel-Mikuš K, Vavpetič P, et al. 2010. Cd induced redistribution of elements within leaves of the Cd/Zn hyperaccumulator

Pongrac P, Vogel-Mikuš K, Regvar M, et al. 2013. On the distribution and evaluation of Na, Mg and Cl in leaves of selected halophytes. Nuclear Instruments and Methods in Physics Research, Section B: Beam Interactions with Materials and Atoms 306: 144–149.

Poschenrieder C, Tolrà R, Barcelo J. 2006. Can meal defend plants against biotic stress? Trends in Plant Science 11: 288–295. PubMed

Pottosin I, Shabala S. 2014. Polyamines control of cation transport across plant membranes: implications for ion homeostasis and abiotic stress signaling. Frontiers in Plant Science 5: 154. PubMed PMC

Pottosin I, Velarde-Buendia AM, Bose J, Fuglsang AT, Shabala S. 2014. Polyamines cause plasma membrane depolarization, activate Ca PubMed

Rabier J, Laffont-Schwob P, Pricop A, et al. 2014. Heavy metal and arsenic resistance of the halophyte

Rastgoo L, Alemzadeh A. 2011. Biochemical responses of Gouan (

Reboreda R, Caçador I. 2007. Halophyte vegetation influences in salt marsh retention capacity for heavy metals. Environmental Pollution 146: 147–154. PubMed

Reboreda R, Caçador I. 2008. Enzymatic activity in the rhizosphere of PubMed

Reboredo 2012. Zinc compartmentation in PubMed

Redondo-Gómez S, Mateos-Naranjo E, Andrades-Moreno L. 2010. Accumulation and tolerance charcateristics of cadmium in a halophytic Cd-hyperaccumulator PubMed

Redondo-Gómez S, Andrades-Moreno L, Mateos-Naranjo E, Parra R, Valera-Burgos J, Aroca R. 2011. Synergic effect of salinity and zinc stress on growth and photosynthetic responses of the cordgrass, PubMed PMC

Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, et al. 2006. Cadmium effect on oxidative metabolism of pea ( PubMed

Rodrigo-Moreno A, Andrés-Colás N, Poschenrieder C, Gunsé B, Peñarrubia L, Shabala S. 2013a. Calcium- and potassium-permeable plasma membrane transporters are activated by copper in Arabidopsis root tips: linking copper transport with cytosolic hydroxyl radical production. Plant, Cell and Environment 36: 844–855. PubMed

Rodrigo-Moreno A, Poschenrieder C, Shabala S. 2013b. Transition metal: a double edge sward in ROS generation and signaling. Plant Signaling & Behaviour 8: e23425. PubMed PMC

Rozema J, Schat H. 2013. Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture. Environmental and Experimental Botany 92: 83–95.

Ruan CJ, Teixeira da Silva J, Mopper S, Qin P, Lutts S. 2010. Halophyte improvement for a salinized world. Critical Review in Plant Sciences 29: 329–359.

Sabey BR, Pendleton RL, Webb BL. 1990. Effect of municipal sewage-sludge application on growth of two reclamation shrub species in copper mine soil. Journal of Environmental Quality 19: 580–586.

Sai Kachout S, Ben Mansoura A, Leclerc JC, Mechergui R, Rejeb MN, Ouerghi Z. 2009. Effects of heavy metals on antioxidant activities of

Sai Kachout SS, Ben Mansoura A, Mechergui R, Leclerc JC, Rejeb MN, Ouerghi Z. 2012. Accumulation of Cu, Pb, Ni and Zn in the halophyte plant PubMed

Saiyood S, Vangnai AS, Inthorn D, Thiravetyan P. 2012. Treatment of total dissolved solids from plastic industrial effluent by halophyte plants. Water, Air and Soil Pollution 223: 4865–4873.

Salt DE, Prince RC, Pickering IJ. 2002. Chemical speciation of accumulated metals in plants: evidence from X-ray absorption spectroscopy. Microchemical Journal 71: 255–259.

Sarret G, Harada E, Choi YE, et al. 2006. Trichomes of tobacco excrete zinc as zinc-substituted calcium carbonate and other zinc-containing compounds. Plant Physiology 141: 1021–1034. PubMed PMC

Sas-Nowosiemska A, Kucharski R, Malkowski E, Pogrzevba M, Kuperberg KM, Kryński K. 2004. Phytoextraction crop disposal – an unsolved problem. Environmental Pollution 128: 373–379. PubMed

Shabala S, Shabala L, Barcelo J, Poschenrieder C. 2014. Membrane transporters mediating root signalling and adaptive resposnes to oxygen deprivation and soil flooding. Plant, Cell and Environment 37: 2216–2233. PubMed

Sharma SS, Dietz KJ. 2006. The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany 57: 711–726. PubMed

Shevyakova NI, Netronina IA, Aronova EE, Kuznetsov VIV. 2003. Compartmentation of cadmium and iron in

Sirguey C, Ouvrad S. 2013. Contaminated soils salinity: a threat for phytoextraction? Chemosphere 91: 269–274. PubMed

Smaoui A, Barhoumi Z, Rabhi M, Abdelly C. 2011. Localization of potential ion transport pathways in vesicular trichome cells of PubMed

Smolders E, Lembregts RM, McLaughlin MJ, Tiller KG. 1998. Effect of soil solution chloride on cadmium availability to Swiss chard. Journal of Environmental Quality 27: 426–431.

Sousa AI, Caçador I, Lillebø AI, Pardal MA. 2008. Heavy metal accumulation in PubMed

Stevens DP, McLaughlin MJ, Heinrich T. 2003. Determining toxicity of lead and zinc runoff in soils: salinity effects on metal partitioning and phytotoxicity. Environmental Toxicology and Chemistry 22: 3017–3024. PubMed

Storey R, Thomson WW. 1994. An X-ray microanalysis study of the salt glands and intracellular crystals of

Storey R, Pitman MG, Stelzer R, Carter C. 1983. X-ray micro-analysis of cells and cell compartments of

Sunby B, Vale C, Caçador I, Catarino F. 1998. Metal-rich concretions on the roots of salt marsh plants: mechanism and rate of formation. Limnology and Oceanography 43: 245–252.

Tate PT, Sik Shin W, Pardue JH, Jackson WA. 2012. Bioremediation of an experimental oil spill in a coastal Louisianna salt marsh. Water, Air and Soil Pollution 223: 1115–1123.

Tauris B, Borg S, Gregersen PL, Holm PB. 2009. A roadmap for zinc trafficking in the developing barley grain based on laser capture microdissection and gene expression profiling. Journal of Experimental Botany 60: 1333–1347. PubMed PMC

Tennstedt P, Peisker D, Böttcher C, Trampczynska A, Clemens S. 2009. Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiology 149: 938–948. PubMed PMC

Thomas JC, Bohnert HJ. 1993. Salt stress perception and plant growth regulators in the halophyte PubMed PMC

Thomas JC, Malick FK, Endreszl C, Davies EC, Murray KS. 1998. Distinct response to copper stress in the halophyte

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.

Usha B, Venkataraman G, Parida A. 2009. Heavy metal and abiotic stress inducible metallothionein isoforms from PubMed

Vahedi A. 2013. The absorption and metabolism of heavy metals and mineral matters in the halophyte plant

Vaillant N, Monnet F, Hitmi A, Sallanon H, Coudret A. 2005. Comparative study of responses in four PubMed

Varga A, Garcinuñ-Martinez RM, Záray G, Fodor F. 1999. Investigations of effects of cadmium, lead, nickel and vanadium contamination on the uptake and transport processes in cucumber plants by TXRF spectrometry.

Vázquez MD, Poschenrieder C, Barceló J, Baker AJM, Hatton P, Cope GH. 1994. Compartmentation of zinc in roots and leaves of the zinc hyperaccumulator

Vogel-Mikuš K, Simčič J, Pelicon P, et al. 2008. Comparison of essential and non-essential element distribution in leaves of the Cd/Zn hyperaccumulator PubMed

Vromman D, Flores-Bavestrello A, Šlejkovec Z, et al. 2011. Arsenic accumulation and distribution in relation to young seedling growth in PubMed

Walker DJ, Lutts S, Sánchez-García M, Correal E. 2014.

Wali M, Ben Rjab K, Gunsé B, et al. 2014. How does NaCl improve tolerance to cadmium in the halophyte PubMed

Wang D, Wang H, Han B, et al. 2012. Sodium instead of potassium and chloride is an important macronutrient to improve leaf succulence and shoot development for halophyte PubMed

Wang HL, Tian CY, Jiang L, Wang L. 2014. Remediation of heavy metals contaminated saline soils: a halophyte choice. Environmental Science and Technology 48: 21–22. PubMed

Weber M, Harada E, Vess C, Roepenack-Lahaye EV, Clemens S. 2004. Comparative microarray analyss of PubMed

Wei W, Chai T, Zhang Y, Han L, Xu J, Guan Z. 2009. The PubMed

Weis J, Weis P. 2004. Metal uptake, transport and release by wetland plants: implications for phytoremediation and restoration. Environment International 169: 737–745. PubMed

Williams JB. 2002. Phytoremediation in wetland ecosystems: progress, problems and potentials. Critical Review in Plant Sciences 21: 607–635.

Wu H, Liu X, Zhao J, Yu J. 2012. Toxicological responses in halophyte PubMed

Wu H, Liu X, Zhao J, Yu J. 2013. Regulation of metabolites, gene expression, and antioxidant enzymes to environmentally relevant lead and zinc in the halophyte

Xu J, Yin H, Liu X, Li X. 2010. Salt affects plant Cd-stress responses by monitoring growth and Cd accumulation. Planta 231: 449–459. PubMed

Yang WE, Long XX, Ye HB, He ZL, Calvert DV, Stoffella PJ. 2004. Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (

Zaier H, Ghnaya T, Lakhdar A, et al. 2010. Comparative study of Pb-phytoextraction potential in PubMed

Zaier H, Ghnaya T, Ghabriche R, et al. 2014. EDTA-enhanced phytoremediation of lead-contaminated soil by the halophyte PubMed

Zepeda-Jazo I, Velarde-Buendía AM, Enríquez-Figueroa R, et al. 2011. Polyamines interact with hydroxyl radicals in activating Ca PubMed PMC

Zhao KF. 1991. Desalinisation of saline soils by

Zimmermann U, Zhu JJ, Meinzer FC, et al. 1994. High molecular weight organic compounds in the xylem sap of mangroves: implication for long distance water transport. Botanica Acta 107: 218–229.

Kosteletzkya pentacarpos: A Potential Halophyte Candidate for Phytoremediation in the Meta(loid)s Polluted Saline Soils

The effect of nanoparticles on the photosynthetic pigments in cadmium-zinc interactions