Abstract
Many areas throughout the world, mainly arid and semi-arid regions, are simultaneously affected by salinity stress and heavy metal (HM) pollution. Phytoremediation of such environments needs suitable plants surviving under those combined stresses. In the present study, native species naturally growing under an extreme condition, around Qaleh-Zari copper mine located in the eastern part of Iran, with HM-contaminated saline–sodic soil, were identified to find suitable plant species for phytoremediation. For this purpose, the accumulation of HMs (Cu, Zn, Cd, and Pb) in the root and shoot (stem and leaf) of the plants and their surrounding soils was determined to find their main phytoremediation strategies: phytoextraction or phytostabilization. Seven native species surviving in such extreme condition were found, including Launaea arborescens (Batt.) Murb, Artemisia santolina Schrenk, Pulicaria gnaphalodes (Vent.) Boiss, Zygophyllum eurypterum Boiss. & Buhse, Peganum harmala L., Pteropyrum olivieri Jaub. & Spach, and Aerva javanica (Burm. f.) Juss. ex Schult. Evaluation of phytoremediation potential of the identified species based on the calculated HM bioconcentration in roots, HM translocation from roots to shoots, and HM accumulation in the shoots revealed that all of the species were metal phytostabilizers rather than hyperaccumulators. Therefore, these native species can be used for phytostabilization in the HM-contaminated saline soils to prevent HMs entering the uncontaminated areas and groundwater. Compared with the biennial low-biomass hyperaccumulators, some native species such as Z. eurypterum and A. javanica may have more economic value for phytoremediation because of a significant accumulation of HMs in their relatively higher biomass.
Similar content being viewed by others
References
Amari T, Ghnaya T, Debez A, Taamali M, Youssef NB, Lucchini G, Sacchi GA, Abdelly C (2014) Comparative Ni tolerance and accumulation potentials between Mesembryanthemum crystallinum (halophyte) and Brassica juncea: metal accumulation, nutrient status and photosynthetic activity. J Plant Physiol 171(17):1634–1644
Amini-Chermahini F, Ebrahimi M, Farajpour M, Taj Bordbar Z (2014) Karyotype analysis and new chromosome number reports in Zygophyllum species. Caryologia 67(4):321–324
Aryafar A, Mohammad Ghasemi T, Ghorbani A (2014) Environmental geophysic and geochemistry studies for investigation of pollutant impacts of drainage of Qaleh Zari copper mine processing plant, South Khorasan. Iran J Min Eng (IRJME) 9(23):81–94
Baindbridge D (2007) A guide for desert and dryland restoration: a new hope for arid lands. Society for Ecological Restoration International. Island Press, Washington
Baker AJ (1981) Accumulators and excluders-strategies in the response of plants to heavy metals. J Plant Nutr 3(1–4):643–654
Beier B-A, Chase M, Thulin M (2003) Phylogenetic relationships and taxonomy of subfamily Zygophylloideae (Zygophyllaceae) based on molecular and morphological data. Plant Syst Evol 240(1):11–39
Ben Rejeb KB, Ghnaya T, Zaier H, Benzarti M, Baioui R, Ghabriche R, Wali M, Lutts S, Abdelly C (2013) Evaluation of the Cd 2+ phytoextraction potential in the xerohalophyte Salsola kali L. and the impact of EDTA on this process. Ecol Eng 60:309–315
Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7(7):1099–1111
Boojar M, Tavakkoli Z (2011) Antioxidative responses and metal accumulation in invasive plant species growing on mine tailings in Zanjan, Iran. Pedosphere 21(6):802–812
Breckle SW, Wucherer W, Dimeyeva LA, Ogar NP (2012) Aralkum-a man-made desert: the desiccated floor of the Aral Sea (Central Asia). Springer, Berlin & Heidelberg
Carter MR, Gregorich EG (2008) Soil sampling and methods of analysis. CRC Press, USA
Chehregani A, Noori M, Yazdi HL (2009) Phytoremediation of heavy-metal-polluted soils: screening for new accumulator plants in Angouran mine (Iran) and evaluation of removal ability. Ecotoxicol Environ Saf 72(5):1349–1353
Christofilopoulos S, Syranidou E, Gkavrou G, Manousaki E, Kalogerakis N (2016) The role of halophyte Juncus acutus L. in the remediation of mixed contamination in a hydroponic greenhouse experiment. J Chem Technol Biotechnol 91(6):1665–1674
Curado G, Rubio-Casal AE, Figueroa E, Castillo JM (2014) Potential of Spartina maritima in restored salt marshes for phytoremediation of metals in a highly polluted estuary. Int J Phytoremediation 16(12):1209–1220
Dalvand M, Hamidian AH, Chahooki Z, Moteshare Zadeh B, Mirjalili S, Esmaeil Zade E (2014) Comparing heavy metal accumulation abilities in Artemisia aucheri and Astragalus gummifer in Darreh Zereshk region, Taft. Desert 19(2):137–140
Ghaderian S, Hemmat G, Reeves R, Baker A (2007) Accumulation of lead and zinc by plants colonizing a metal mining area in Central Iran. J Appl Bot Food Qual 81(2):145–150
Ghahraman A (1975-2000) Colored flora of Iran, 1-22 edn. Research Inistitute of Forests and Rangelands, Tehran
Ghnaya T, Nouairi I, Slama I, Messedi D, Grignon C, Abdelly C, Ghorbel MH (2005) Cadmium effects on growth and mineral nutrition of two halophytes: Sesuvium portulacastrum and Mesembryanthemum crystallinum. J Plant Physiol 162(10):1133–1140
Ghrabi Z (2005) A guide to medicinal plants in North Africa. IUCN Centre for Mediterranean Cooperation, Malaga
Idaszkin YL, Lancelotti JL, Pollicelli MP, Marcovecchio JE, Bouza PJ (2017) Comparison of phytoremediation potential capacity of Spartina densiflora and Sarcocornia perennis for metal polluted soils. Mar Pollut Bull 118(1–2):297–306
Kabata-Pendias A (2011) Trace elements in soils and plants. CRC press, USA
Kachout SS, Mansoura AB, Mechergui R, Leclerc JC, Rejeb MN, Ouerghi Z (2012) Accumulation of Cu, Pb, Ni and Zn in the halophyte plant Atriplex grown on polluted soil. J Sci Food Agric 92(2):336–342
Kadukova J, Manousaki E, Kalogerakis N (2008) Pb and Cd accumulation and phyto-excretion by salt cedar (Tamarix smyrnensis Bunge). Int J Phytoremediation 10(1):31–46
Kamkar A, Ardekani MRS, Shariatifar N, Misagi A, Nejad ASM, Jamshidi AH (2013) Antioxidative effect of Iranian Pulicaria gnaphalodes L. extracts in soybean oil. S Afr J Bot 85:39–43
Karam MA, Abd-Elgawad ME, Ali RM (2016) Differential gene expression of salt-stressed Peganum harmala L. J Gen Eng Biotechnol 14(2):319–326
Khan MA (2003) An ecological overview of halophytes from Pakistan. In: Lieth H, Mochtchenko M (eds) Cash crop halophytes: recent studies. Springer Science & Business Media, B. V
Khan MA, Böer B, Kust GS, Barth HJ (2006) Sabkha ecosystems: volume II: West and Central Asia. Springer, Netherlands
Khan MA, Ozturk M, Gul B, Ahmed MZ (2015) Halophytes for food security in dry lands. Academic Press
Klute A (1986) Methods of soil analysis. Part 1. Physical and mineralogical methods. American Society of Agronomy Inc. Madison, Wisconsin, USA.
Korzeniowska J, Stanislawska-Glubiak E (2015) Phytoremediation potential of Miscanthus × giganteus and Spartina pectinata in soil contaminated with heavy metals. Environ Sci Pollut Res 22(15):11648–11657
Liang L, Liu W, Sun Y, Huo X, Li S, Zhou Q (2017) Phytoremediation of heavy metal contaminated saline soils using halophytes: current progress and future perspectives. Environ Rev 999:1–13
Lu Y, Li X, He M, Zhao X, Liu Y, Cui Y, Pan Y, Tan H (2010) Seedlings growth and antioxidative enzymes activities in leaves under heavy metal stress differ between two desert plants: a perennial (Peganum harmala) and an annual (Halogeton glomeratus) grass. Acta Physiol Plant 32(3):583–590
Lutts S, Lefevre I (2015) How can we take advantage of halophyte properties to cope with heavy metal toxicity in salt-affected areas? Ann Bot 115(3):509–528
Manousaki E, Kalogerakis N (2011) Halophytes present new opportunities in phytoremediation of heavy metals and saline soils. Ind Eng Chem Res 50(2):656–660
Manousaki E, Kadukova J, Papadantonakis N, Kalogerakis N (2008) Phytoextraction and phytoexcretion of Cd by the leaves of Tamarix smyrnensis growing on contaminated non-saline and saline soils. Environ Res 106(3):326–332
Manousaki E, Galanaki K, Papadimitriou L, Kalogerakis N (2014) Metal phytoremediation by the halophyte Limoniastrum monopetalum (L.) Boiss: two contrasting ecotypes. Int J Phytoremediation 16(7–8):755–769
Marrugo-Negrete J, Marrugo-Madrid S, Pinedo-Hernández J, Durango-Hernández J, Díez S (2016) Screening of native plant species for phytoremediation potential at a Hg-contaminated mining site. Sci Total Environ 542:809–816
Marschner P (2012) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, USA
Mbagwu J, Mbah C (1998) Estimating water retention and availability in Nigerian soils from their saturation percentage. Commun Soil Sci Plant Anal 29(7–8):913–922
Milić D, Luković J, Ninkov J, Zeremski-Škorić T, Zorić L, Vasin J, Milić S (2012) Heavy metal content in halophytic plants from inland and maritime saline areas. Open Life Sciences 7(2):307–317
Mousavi Kouhi SM, Lahouti M, Ganjeali A, Entezari MH (2015) Comparative effects of ZnO nanoparticles, ZnO bulk particles, and Zn2+ on Brassica napus after long-term exposure: changes in growth, biochemical compounds, antioxidant enzyme activities, and Zn bioaccumulation. Water Air Soil Pollut 226:364–373
Mozaffarian V (1996) A dictionary of Iranian plant names: Latin, English, Persian. Farhang Mo'aser, Iran
Naseem S, Bashir E, Shireen K, Shafiq S (2009) Soil-plant relationship of Pteropyrum olivieri, a serpentine flora of Wadh, Balochistan, Pakistan and its use in mineral prospecting. Studia UBB Geologia 54(2):33–39
Nezhadali A, Lari J, Asili J, Mahmoudabadi M (2010) Chemical composition of the essential oil of Artemisia santolina. J Essent Oil Bear Plants 13(6):738–741
Nouri J, Lorestani B, Yousefi N, Khorasani N, Hasani A, Seif F, Cheraghi M (2011) Phytoremediation potential of native plants grown in the vicinity of Ahangaran lead–zinc mine (Hamedan, Iran). Environ Earth Sci 62(3):639–644
Page AL, Miller RH, and Keeney DR (1994) Methods of soil analysis. Part 2. Chemical and microbiological properties. Soil Science Society of America, Inc, USA.
Palmer J, Lally TR (2011) Amaranthaceae. In: Kellermann J (ed) Flora of South Australia. State Herbarium of South Australia, Adelaide, pp 1–42
Peacock WL, Christensen LP (2000) Interpretation of soil and water analysis. In: Christensen LP (ed) raisin production manual, 3393rd edn. University of California ANR Publication, Canada, pp 115–120
Phondani PC, Bhatt A, Elsarrag E, Alhorr YM (2015) Seed germination and growth performance of Aerva javanica (Burm.f.) Juss ex Schult. J Appl Res Med Aromat Plants 2(4):195–199
Piri Sahragard H, Zare Chahuoki MA, Azarnivand H (2016) Developing predictive distribution map of plant species habitats using logistic regression (case study: Khalajestan rangelands of Qum province). J Rangeland Sci 9(3):222–234
Rajaganapathy V, Xavier F, Sreekumar D, Mandal PK (2011) Heavy metal contamination in soil, water and fodder and their presence in livestock and products : a review. J Environ Sci Technol 4:234–249
Rhoades JD (1982) Soluble salts. In: Page AL(ed) methods of soil analysis: part 2: chemical and microbiological properties, 2nd edn. Amer Society of Agronomy, Madison, pp 167–179
Richards LA (1954) Diagnosis and improvements of saline and alkali soils. US Deptartment of Agriculture, Washington
Sadeghi Benis M, Hassani A, Nouri J, Mehregan I, Moattar F (2015) The effect of soil properties and plant species on the absorption of heavy metals in industrial sewage contaminated soil: a case study of Eshtehard Industrial Park. Bulg Chem Commun 47:211–219
Samejo MQ, Memon S, Bhanger MI, Khan KM (2012) Chemical compositions of the essential oil of Aerva javanica leaves and stems. Pak J Anal Environ Chem 13(1):48–52
Santos E, Abreu M, Peres S, Magalhães M, Leitão S, Pereira A, Cerejeira M (2017) Potential of Tamarix africana and other halophyte species for phytostabilisation of contaminated salt marsh soils. J Soils Sediments 17(5):1459–1473
Schütz W, Milberg P (1997) Seed germination in Launaea arborescens: a continuously flowering semi-desert shrub. J Arid Environ 36(1):113–122
Sharma A, Gontia I, Agarwal PK, Jha B (2010) Accumulation of heavy metals and its biochemical responses in Salicornia brachiata, an extreme halophyte. Mar Biol Res 6(5):511–518
Sumner ME (1993) Sodic soils-new perspectives. Soil Research 31(6):683–750
Taiz L, Zeiger E (2002) Plant physiology. Sinauer Associates, Sunderland
Tavakkoli E, Rengasamy P, McDonald GK (2010) High concentrations of Na+ and Cl− ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. J Exp Bot 61(15):4449–4459
Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. Experientia Supplementum 101:133–164
Uddin AH, Khalid RS, Alaama M, Abdualkader AM, Kasmuri A, Abbas S (2016) Comparative study of three digestion methods for elemental analysis in traditional medicine products using atomic absorption spectrometry. J Anal Sci Technol 7(1):6
Van Oosten MJ, Maggio A (2015) Functional biology of halophytes in the phytoremediation of heavy metal contaminated soils. Environ Exp Bot 111:135–146
Wang H-L, Tian C-Y, Jiang L, Wang L (2014) Remediation of heavy metals contaminated saline soils: a halophyte choice? Environ Sci Technol 48(1):21–22
Wright CW (2002) Artemisia, medicinal and aromatic plants—industrial profiles. Taylor and Francis, London
Zhao F, Lombi E, McGrath S (2003) Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulator Thlaspi caerulescens. Plant Soil 249(1):37–43
Acknowledgments
The authors are grateful to the research council of the University of Birjand for financial support under contract number 1395/d/23532.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
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
Mousavi Kouhi, S.M., Moudi, M. Assessment of phytoremediation potential of native plant species naturally growing in a heavy metal-polluted saline–sodic soil. Environ Sci Pollut Res 27, 10027–10038 (2020). https://doi.org/10.1007/s11356-019-07578-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-07578-6