Assessment of phytoremediation potential of native plant species naturally growing in a heavy metal-polluted saline–sodic soil

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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.

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  1. 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

  2. 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

  3. 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

  4. Baindbridge D (2007) A guide for desert and dryland restoration: a new hope for arid lands. Society for Ecological Restoration International. Island Press, Washington

  5. Baker AJ (1981) Accumulators and excluders-strategies in the response of plants to heavy metals. J Plant Nutr 3(1–4):643–654

  6. 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

  7. 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

  8. Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7(7):1099–1111

  9. 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

  10. 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

  11. Carter MR, Gregorich EG (2008) Soil sampling and methods of analysis. CRC Press, USA

  12. 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

  13. 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

  14. 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

  15. 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

  16. 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

  17. Ghahraman A (1975-2000) Colored flora of Iran, 1-22 edn. Research Inistitute of Forests and Rangelands, Tehran

  18. 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

  19. Ghrabi Z (2005) A guide to medicinal plants in North Africa. IUCN Centre for Mediterranean Cooperation, Malaga

  20. 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

  21. Kabata-Pendias A (2011) Trace elements in soils and plants. CRC press, USA

  22. 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

  23. 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

  24. 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

  25. 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

  26. 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

  27. Khan MA, Böer B, Kust GS, Barth HJ (2006) Sabkha ecosystems: volume II: West and Central Asia. Springer, Netherlands

  28. Khan MA, Ozturk M, Gul B, Ahmed MZ (2015) Halophytes for food security in dry lands. Academic Press

  29. Klute A (1986) Methods of soil analysis. Part 1. Physical and mineralogical methods. American Society of Agronomy Inc. Madison, Wisconsin, USA.

  30. 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

  31. 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

  32. 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

  33. 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

  34. 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

  35. 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

  36. 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

  37. 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

  38. Marschner P (2012) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, USA

  39. 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

  40. 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

  41. 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

  42. Mozaffarian V (1996) A dictionary of Iranian plant names: Latin, English, Persian. Farhang Mo'aser, Iran

  43. 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

  44. 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

  45. 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

  46. 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.

  47. Palmer J, Lally TR (2011) Amaranthaceae. In: Kellermann J (ed) Flora of South Australia. State Herbarium of South Australia, Adelaide, pp 1–42

  48. 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

  49. 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

  50. 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

  51. 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

  52. 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

  53. Richards LA (1954) Diagnosis and improvements of saline and alkali soils. US Deptartment of Agriculture, Washington

  54. 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

  55. 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

  56. 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

  57. Schütz W, Milberg P (1997) Seed germination in Launaea arborescens: a continuously flowering semi-desert shrub. J Arid Environ 36(1):113–122

  58. 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

  59. Sumner ME (1993) Sodic soils-new perspectives. Soil Research 31(6):683–750

  60. Taiz L, Zeiger E (2002) Plant physiology. Sinauer Associates, Sunderland

  61. 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

  62. Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. Experientia Supplementum 101:133–164

  63. 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

  64. Van Oosten MJ, Maggio A (2015) Functional biology of halophytes in the phytoremediation of heavy metal contaminated soils. Environ Exp Bot 111:135–146

  65. 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

  66. Wright CW (2002) Artemisia, medicinal and aromatic plants—industrial profiles. Taylor and Francis, London

  67. 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

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The authors are grateful to the research council of the University of Birjand for financial support under contract number 1395/d/23532.

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Correspondence to Seyed Mousa Mousavi Kouhi.

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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 (2020) doi:10.1007/s11356-019-07578-6

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  • Extreme environment
  • Halophyte
  • Metal contamination
  • Phytoextraction
  • Phytostabilization
  • Salinity