Advertisement

Heavy Metal Tolerance in Two Algerian Saltbushes: A Review on Plant Responses to Cadmium and Role of Calcium in Its Mitigation

  • Bouzid Nedjimi
Chapter

Abstract

Heavy metal pollution is a common environmental constraint to human health. The physicochemical decontamination constitutes a high costly procedure and not practicable in extensive polluted soils. Therefore, selecting plants naturally tolerant to heavy metals is an alternative approach for a sustainable phytoremediation. The aptitude of species to tolerate heavy metals is determined by several biochemical trails that protect photosynthetic apparatus and maintain growth and chemical elements homeostasis. Cadmium (Cd) is a high toxic environmental pollutant and can interfere with various metabolic processes such as photosynthesis, respiration, and mineral uptake and some enzymatic activities that are crucial for plant growth. Atriplex halimus L. and A. nummularia L. (Amaranthaceae) are two widespread saltbushes used for desalination and rehabilitation of Algerian saline lands. These shrubs have a high biomass production, extensive root system, low nutrient requirements, and easy propagation, among other benefits. Calcium (Ca) supplementation was largely used to improve heavy metal tolerance of plant species. Ca is an indispensable element for plant growth, membrane integrity, osmotic adjustment, and signaling transduction. Exogenous application of this element can play a significant role to enhance plant tolerance against Cd toxicity. This chapter reviews the tolerance of A. halimus and A. nummularia saltbushes to Cd stress and the impact of this heavy metal on physiological and biochemical traits. In addition the beneficial role of Ca supplementation to alleviating Cd toxicity in these species was discussed.

Keywords

Atriplex sp. Cadmium toxicity Calcium addition Halophytes Heavy metals Phytoextraction Phytostabilization Pollution 

Notes

Acknowledgment

All researches were funded by the Algerian National Program of Research, CNEPRU Project code # D04N01UN170120140017.

References

  1. Ahmad I, Maathuis FJM (2014) Cellular and tissue distribution of potassium; physiological relevance, mechanisms and regulation. J Plant Physiol 171:708–714CrossRefPubMedPubMedCentralGoogle Scholar
  2. Antosiewicz D, Hennig J (2004) Overexpression of LCT1 in tobacco enhances the protective action of calcium against cadmium toxicity. Environ Pollut 129:237–245CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216CrossRefGoogle Scholar
  4. Ashraf MY, Sadiq R, Hussain M, Ashraf M, Ahmad MSA (2011) Toxic effect of nickel (Ni) on growth and metabolism in germinating seeds of sunflower (Helianthus annuus L.) Biol Trace Elem Res 143:1695–1703CrossRefPubMedPubMedCentralGoogle Scholar
  5. Asp H, Gussarsson M, Adalsteinson S, Lensén P (1994) Control of potassium influx in roots of birch (Betula pendula) seedlings exposed to cadmium. J Exp Bot 45:1823–1827CrossRefGoogle Scholar
  6. Aydinalp C, Marinova S (2009) The effects of heavy metals on seed germination and plant growth on alfalfa plant (Medicago sativa). Bulg J Agri Sci 15:347–350Google Scholar
  7. Ayyappan D, Sathiyaraj G, Ravindran KC (2016) Phytoextraction of heavy metals by Sesuvium portulacastrum a salt marsh halophyte from tannery effluent. Int J Phytoremediation 18:453–459CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bankaji I, Caçador I, Sleimi N (2015) Physiological and biochemical responses of Suaeda fruticosa to cadmium and copper stresses: growth, nutrient uptake, antioxidant enzymes, phytochelatin, and glutathione levels. Environ Sci Pollut Res 22:13058–13069CrossRefGoogle Scholar
  9. Barakat NAM, Laudadio V, Nedjimi B, Kabiel HF, Tufarelli V (2013) Ecophysiological and species-specific responses to seasonal variations in halophytic species of the Chenopodiaceae in a Mediterranean salt marsh. Afr J Ecol 52:163–172CrossRefGoogle Scholar
  10. Bertrand M, Poirier I (2005) Photosynthetic organisms and excess of metals. Photosynthetica 43:345–353CrossRefGoogle Scholar
  11. 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. South Afr J Bot 85:63–69CrossRefGoogle Scholar
  12. Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719CrossRefPubMedPubMedCentralGoogle Scholar
  13. Das P, Samantaray S, Rout GR (1997) Studies on cadmium toxicity in plants: a review. Environ Pollut 98:29–36CrossRefPubMedPubMedCentralGoogle Scholar
  14. Deng G, Li M, Li H, Yin L, Li W (2014) Exposure to cadmium causes declines in growth and photosynthesis in the endangered aquatic fern (Ceratopteris pteridoides). Aquat Bot 112:23–32CrossRefGoogle Scholar
  15. Dias MC, Monteiro C, Moutinho-Pereira J, Correia C, Gonçalves B, Santos C (2012) Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiol Plant 35:1281–1289CrossRefGoogle Scholar
  16. Drążkiewicz M, Baszyński T (2008) Calcium protection of PS2 complex of Phaseolus coccineus from cadmium toxicity: in vitro study. Environ Exp Bot 64:8–14CrossRefGoogle Scholar
  17. Eissa MA (2015) Impact of compost on metals phytostabilization potential of two halophytes species. Int J Phytoremediation 17:662–668CrossRefPubMedPubMedCentralGoogle Scholar
  18. El-Enany AE (1995) Alleviation of cadmium toxicity on maize seedlings by calcium. Biol Plant 37:93–99CrossRefGoogle Scholar
  19. Faller P, Kienzler K, Krieger-Liszkay A (2005) Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of photosystem II by competitive binding to the essential Ca2+ site. Biochim Biophys Acta 1706:158–164CrossRefPubMedPubMedCentralGoogle Scholar
  20. Farzadfar S, Zarinkamar F, Modarres-Sanavy SAM, Hojati M (2013) Exogenously applied calcium alleviates cadmium toxicity in Matricaria chamomilla L. plants. Environ Sci Pollut Res 20:1413–1422CrossRefGoogle Scholar
  21. 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 162:1133–1140CrossRefPubMedGoogle Scholar
  22. Ghnaya T, Slama I, Messedi D, Grignon C, Ghorbe MH, Abdelly C (2007) Effects of Cd2+ on K+, Ca2+ and N uptake in two halophytes Sesuvium portulacastrum and Mesembryanthemum crystallinum: consequences on growth. Chemosphere 67:72–79CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hasanuzzaman M, Fujita M (2012) Heavy metals in the environment: current status, toxic effects on plants and possible phytoremediation. In: Anjum NA, Pereira MA, Ahmad I, Duarte AC, Umar S, Khan NA (eds) Phytotechnologies: remediation of environmental contaminants. CRC, Boca Raton, pp 7–73CrossRefGoogle Scholar
  24. Hasanuzzaman M, Nahar K, Alam MM, Bhowmi, Hossain MA, Rahman MM, Prasad MNV, Ozturk M, Fujita M (2014) Potential use of halophytes to remediate saline soils. Bio Med Resh Int 2014:12.  https://doi.org/10.1155/2014/589341 CrossRefGoogle Scholar
  25. Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017a) Exogenous silicon attenuates cadmium-induced oxidative stress in Brassica napus L. by modulating AsA-GSH pathway and glyoxalase system. Front Plant Sci 8:1061.  https://doi.org/10.3389/fpls.2017.01061 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hasanuzzaman M, Nahar K, Gill SS, Alharby HF, Razafindrabe BHN, Fujita M (2017b) Hydrogen peroxide pretreatment mitigates cadmium-induced oxidative stress in Brassica napus L.: an intrinsic study on antioxidant defense and glyoxalase systems. Front Plant Sci 8:115.  https://doi.org/10.3389/fpls.2017.00115 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hashem A, E, Abd-Allah F, Alqarawi AA, Malik JA, Wirth S, Egamberdieva D (2017) Role of calcium in AMF-mediated alleviation of the adverse impacts of cadmium stress in Bassia indica [Wight] A. J. Scott. Saudi J Biol Sci.  https://doi.org/10.1016/j.sjbs.2016.11.003
  28. Hsu FH, Chou CH (1992) Inhibitory effect of heavy metals on seed germination and seedling growth of Miscanthus species. Bot Bull Acad Sci 33:335–342Google Scholar
  29. Huang D, Gong X, Liu Y, Zeng G, Lai C, Bashir H, Zhou L, Wang D, Xu P, Cheng M, Wan J (2017) Effects of calcium at toxic concentrations of cadmium in plants. Planta 245:863–873CrossRefPubMedGoogle Scholar
  30. Huebert DB, Shay JM (1991) The effect of cadmium and its interaction with external calcium in the submerged aquatic macrophyte Lemna trisulca L. Aquat Toxicol 20:57–71CrossRefGoogle Scholar
  31. Kabata–Pendias A (2004) Soil–plant transfer of trace elements–an environmental issue. Geoderma 122:143–149CrossRefGoogle Scholar
  32. Kirkham MB (2006) Cadmium in plants on polluted soils: effects of soil factors, hyperaccumulation, and amendments. Geoderma 137:19–32CrossRefGoogle Scholar
  33. Kramer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534CrossRefPubMedPubMedCentralGoogle Scholar
  34. Küpper H, Küpper F, Spiller M (1998) In situ detection of heavy metal substituted chlorophylls in water plants. Photosynth Res 58:123–133CrossRefGoogle Scholar
  35. Le Houérou H (1992) The role of saltbushes (Atriplex sp.) in arid land rehabilitation in the mediteranean bassin: a review. Agrofor Syst 18:107–146CrossRefGoogle Scholar
  36. Li L, Liu X, Peijnenburg WJGM, Zhao J, Chen X, Yu J, Wu H (2012) Pathways of cadmium fluxes in the root of the halophyte Suaeda salsa. Ecotox Environ Saf 75:1–7CrossRefGoogle Scholar
  37. Li P, Zhao C, Zhang Y, Wang X, Wang J, Wang F, Bi Y (2016) Calcium alleviates cadmium-induced inhibition on root growth by maintaining auxin homeostasis in Arabidopsis seedlings. Protoplasma 253:185–200CrossRefPubMedPubMedCentralGoogle Scholar
  38. Liu S, Yang C, Xie W, Xia C, Fan P (2012) The effects of cadmium on germination and seedling growth of Suaeda salsa. Procedia Environ Sci 16:293–298CrossRefGoogle Scholar
  39. Lomonte C, Sgherri C, Baker AJM, Kolev SD, Navari-Izzo F (2010) Antioxidative response of Atriplex codonocarpa to mercury. Environ Exp Bot 69:9–16CrossRefGoogle Scholar
  40. 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 115:509–528CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lutts S, Lefèvre I, Délperée C, Kivits S, Dechamps C, Robledo A, Correal E (2004) Heavy metal accumulation by the halophyte species Mediterranean saltbush. J Environ Qual 33:1271–1279CrossRefPubMedPubMedCentralGoogle Scholar
  42. Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37CrossRefPubMedPubMedCentralGoogle Scholar
  43. Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84:123–133CrossRefGoogle Scholar
  44. Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13CrossRefGoogle Scholar
  45. Manousaki E, Kalogeraki N (2011) Halophytes present new opportunities in phytoremediation of heavy metals and saline soils. Ind Eng Chem Res 50:656–660CrossRefGoogle Scholar
  46. Márquez-García B, Márquez C, Sanjosé I, Nieva FJJ, Rodríguez-Rubio P, Muñoz-Rodríguez AF (2013) The effects of heavy metals on germination and seedling characteristics in two halophyte species in Mediterranean marshes. Mar Poll Bull 70:119–124CrossRefGoogle Scholar
  47. Meng H, Hua S, Shamsi IH, Jilani G, Li Y, Jiang L (2009) Cadmium-induced stress on the seed germination and seedling growth of Brassica napus L., and its alleviation through exogenous plant growth regulators. Plant Growth Regul 58:47–59CrossRefGoogle Scholar
  48. Nedjimi B (2009) Calcium can protect Atriplex halimus subsp. schweinfurthii from cadmium toxicity. Acta Bot Gallica 156:391–397CrossRefGoogle Scholar
  49. Nedjimi B (2013) Involvement of proline in plant response to salt stress. In: Nedjimi B (ed) Proline: biosynthesis, regulation and health benefits. Nova Science Publishers, New York, pp 1–9Google Scholar
  50. Nedjimi B, Daoud Y (2009) Cadmium accumulation in Atriplex halimus subsp. schweinfurthii and its influence on growth, proline, root hydraulic conductivity and nutrient uptake. Flora 204:316–324CrossRefGoogle Scholar
  51. Nedjimi B, Guit B, Toumi M, Beladel B, Akam A, Daoud Y (2013) Atriplex halimus subsp. schweinfurthii (Chenopodiaceae): description, écologie et utilités pastorales et thérapeutiques. Rev Four 216:333–338Google Scholar
  52. Nedjimi B, Mohammedi N, Belkheiri S (2014) Germination responses of medic tree (Medicago arborea) seeds to salinity and temperature. Agricultural Res 3:308–312CrossRefGoogle Scholar
  53. Nirmal Kumar IJ, Sajish PR, Nirmal Kumar R, Basil G, Shailendra V (2011) An assessment of the accumulation potential of Pb, Zn and Cd by Avicennia marina (Forssk.) Vierh. in Vamleshwar mangroves, Gujarat, India. Not Sci Biol 3:36–40CrossRefGoogle Scholar
  54. Ouzonidou G, Moustakas M, Eleftheriou EP (1997) Physiological and ultrastructural effects of cadmium on wheat (Triticum aestivum L.) leaves. Arch Environ Contam Toxicol 32:154–160CrossRefGoogle Scholar
  55. Prakash JSS, Baig MA, Bhagwat AS, Mohanty P (2003) Characterisation of senescence induced changes in light harvesting complex II and photosystem I complex of thylakoids of Cucumis sativus cotyledons: age induced association of LHC II with photosystem I. J Plant Physiol 160:175–184CrossRefPubMedPubMedCentralGoogle Scholar
  56. Rastgoo L, Alemzadeh A (2011) Biochemical responses of Gouan (Aeluropus littoralis) to heavy metal stress. Aus J Crop Sci 5:375–383Google Scholar
  57. Saïdani E, Nedjimi B (2014) Effet du chrome hexavalent (K2CrO7) sur la germination d’Atriplex halimus L. BioRessources 4:47–52CrossRefGoogle Scholar
  58. Sakouhi L, Rahoui S, Ben Massoud M, Munemasa S, EL Ferjani E, Murata Y, Chaoui A (2016) Calcium and EGTA alleviate cadmium toxicity in germinating chickpea seeds. J Plant Growth Regul 35:1064–1073CrossRefGoogle Scholar
  59. Sanitá di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130CrossRefGoogle Scholar
  60. Sawalha MF, Peralta-Videa JR, Romeor-Gonzalez J, Gardea-Torresdey JL (2006) Biosorption of Cd(II), Cr(II) and Cr(VI) by saltbush (Atriplex carnescens) biomass: thermodynamic and isotherm studies. Colloid Interf Sci 300:100–104CrossRefGoogle Scholar
  61. Schat H, Sharma SS, Vooijs R (1997) Heavy metal-induced accumulation of free proline in a metal-tolerant and a non-tolerant ecotype of Silene vulgaris. Physiol Plant 101:477–482CrossRefGoogle Scholar
  62. Schmidke I, Stephan UW (1995) Transport of metal micronutrients in the phloem of castor bean (Ricinus communis) seedlings. Physiol Plant 95:147–153CrossRefGoogle Scholar
  63. Sethy SK, Ghosh S (2013) Effect of heavy metals on germination of seeds. J Nat Sci Biol Med 4:272–275CrossRefPubMedPubMedCentralGoogle Scholar
  64. Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726CrossRefPubMedPubMedCentralGoogle Scholar
  65. 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 6:511–518CrossRefGoogle Scholar
  66. Shevyakova NI, Netronina IA, Aronova EE, Kuznetsov VV (2003) Compartmentation of cadmium and iron in Mesembryanthemum crystallinum plants during the adaptation to cadmium stress. Russ J Plant Physiol 50:678–685CrossRefGoogle Scholar
  67. Shi HP, Zhu YF, Wang YL, Tsang PKE (2014) Effect of cadmium on cytogenetic toxicity in hairy roots of Wedelia trilobata L. and their alleviation by exogenous CaCl2. Environ Sci Pollut Res 21:1436–1443CrossRefGoogle Scholar
  68. Silveira JAG, Araújo SAM, Lima JPMS, Viégas RA (2009) Roots and leaves display contrasting osmotic adjustment mechanisms in response to NaCl-salinity in Atriplex nummularia. Environ Exp Bot 66:1–8CrossRefGoogle Scholar
  69. Sivaci ER, Sivaci A, Sökmen M (2004) Biosorption of cadmium by Myriophyllum spicatum and Myriophyllum triphyllum orchard. Chemosphere 56:1043–1048CrossRefPubMedGoogle Scholar
  70. Solís-Domínguez FA, González-Chávez MC, Carrillo-González R, Rodríguez-Vázquez R (2007) Accumulation and localization of cadmium in Echinochloa polystachya grown within a hydroponic system. J Haz Mat 141:630–636CrossRefGoogle Scholar
  71. Stolt JP, Sneller FEC, Brynelsson T, Lundborg T, Schat H (2003) Phytochelatin and cadmium accumulation in wheat. Environ Exp Bot 49:21–28CrossRefGoogle Scholar
  72. Susarla S, Medina VF, McCutcheon SC (2002) Phytoremediation: an ecological solution to organic chemical contamination. Ecol Eng 18:647–658CrossRefGoogle Scholar
  73. Suzuki N (2005) Alleviation by calcium of Cd-induced root growth inhibition in Arabidopsis seedling. Plant Biotechnol 22:19–25CrossRefGoogle Scholar
  74. Talebi S, Kalat SMN, Darban ALS (2014) The study effects of heavy metals on germination characteristics and proline content of Triticale (Triticosecale Wittmack). Int J Farm Alli Sci 3:1080–1087Google Scholar
  75. Talukdar D (2012) Exogenous calcium alleviates the impact of cadmium-induced oxidative stress in Lens culinaris medic seedlings through modulation of antioxidant enzyme activities. J Crop Sci Biotech 15:325–334CrossRefGoogle Scholar
  76. Tian S, Lu L, Zhang J, Wang K, Brown P, He Z, Liang J, Yang X (2011) Calcium protects roots of Sedum alfredii H. against cadmium-induced oxidative stress. Chemosphere 84:163–169Google Scholar
  77. Vromman D, Flores-Bavestrello A, Šlejkovec Z, Lapaille S, Teixeira-Cardoso C, Briceño M, Kumar M, Martínez J-P, Lutts S (2011) Arsenic accumulation and distribution in relation to young seedling growth in Atriplex atacamensis Phil. Sci Total Environ 412:286–295CrossRefPubMedPubMedCentralGoogle Scholar
  78. Wang CQ, Song H (2009) Calcium protects Trifolium repens L. seedlings against cadmium stress. Plant Cell Rep 28:1341–1349CrossRefPubMedPubMedCentralGoogle Scholar
  79. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511CrossRefPubMedPubMedCentralGoogle Scholar
  80. Wierzbicka M, Obidzinska J (1998) The effect of lead on seed imbibition and germination in different plant species. Plant Sci 137:155–171CrossRefGoogle Scholar
  81. Wu G, Kang H, Zhang X, Shao H, Chu L, Ruan C (2010) A critical review on the bio– removal of hazardous heavy metals from contaminated soils: issues, progress, eco–environmental concerns and opportunities. J Haz Mat 174:1–8CrossRefGoogle Scholar
  82. Zhao FJ, Jiang RF, Dunham SJ, McGrath SP (2006) Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri. New Phytol 172:646–654CrossRefPubMedPubMedCentralGoogle Scholar
  83. Zhenyan HE, Jiangchuan LI, Zhang H, Ma MI (2005) Different effects of calcium and lanthanum on the expression of phytochelatin synthase gene and cadmium absorption in Lactuca sativa. Plant Sci 168:309–318CrossRefGoogle Scholar
  84. Zouaria M, Ben Ahmed C, Zorrig W, Elloumi N, Rabhi M, Delmail D, Ben Rouina B, Labrousse P, Ben Abdallah F (2016) Exogenous proline mediates alleviation of cadmium stress by promoting photosynthetic activity, water status and antioxidative enzymes activities of young date palm (Phoenix dactylifera L.) Ecotoxicol Environ Saf 128:100–108CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Bouzid Nedjimi
    • 1
  1. 1.Laboratory of Exploration and Valorization of Steppe Ecosystem, Faculty of Science of Nature and LifeUniversity of DjelfaDjelfaAlgeria

Personalised recommendations