Phytoremediation and Rhizoremediation: Uptake, Mobilization and Sequestration of Heavy Metals by Plants

  • Smita S. Kumar
  • Abudukeremu Kadier
  • Sandeep K. Malyan
  • Altaf Ahmad
  • Narsi R. BishnoiEmail author


Microorganisms residing over the rhizosphere have the capability to catalyse metal uptake in a symbiotic relationship with the roots. This syntrophic relationship enhances the bioavailability of heavy metals and encourages the root adsorption capacity for vital in addition to non-essential metal. It also changes their chemical properties that ultimately have an effect on metal dissolution. Molecular level understanding of the physiological and evolutionary mechanism along with genetics and biochemistry principles underlying the uptake, transportation, translocation and storage of heavy metals (HMs) in model plant species thus allowing alteration to the HM stress can loan much to our comprehension of the fundamental segments of HM metabolism. A lucid understanding of molecular level changes is necessary for plant biotechnologist, regarding changes provoked in plants because of HM stress. It is also helpful to develop stress-resistant cultivars and species with superior phytoremediation capacity through cell and genetic engineering technologies. We hereby summarize the present understanding of HM uptake by plants and also provide a brief study related to their biochemical characteristics of take-up, transport and assortment plus injury and defence mechanism against HM. In this review chapter, we have also focused over the future prospect of research to enhance the discriminate perspective of the basic phytoremediation components specifically rhizoremediation of HMs.


Rhizoremediation Heavy metals Sequestration Phytoremediation Heavy metal detoxification 



The first author is grateful to the University Grant Commission and Basic Scientific Research, New Delhi, for the financial grant.


  1. Abou-Shanab RA, Angle JS, Delorme TA, Chaney RL, van Berkum P, Moawad H, Ghanem K, Ghozlan HA (2003) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158:219–224CrossRefGoogle Scholar
  2. Al-Agely A, Sylvia DM, Ma LQ (2005) Mycorrhizae increase arsenic uptake by the hyperaccumulator Chinese brake fern (Pteris vittata L.) J Environ Qual 34:2181–2186PubMedCrossRefGoogle Scholar
  3. Anjum NA, Ahmad I, Mohmood I, Duarte AC, Pereira E, Umae S, Ahmad A, Khand NA, Iqbal M, Prasad MNV (2012) Modulation of glutathione and its related enzymes in plants responses to toxic metals and metalloids–a review. Environ Exp Bot 75:307–324Google Scholar
  4. Anwar HM, Garcia-Sanchez A, Alam Tari Kul M, Majibur Rahman M (2008) Phytofiltration of water polluted with arsenic and heavy metals. Int J Environ Pollut 33:292–312CrossRefGoogle Scholar
  5. Astier J, Kulik A, Koen E, Besson-Bard A, Bourque S, Jeandroz S, Lamotte O, Wendehenne D (2012) Protein S-nitrosylation: what’s going on in plants? Free Radic Biol Med 53:1101–1110PubMedCrossRefGoogle Scholar
  6. Atimanav G, Alok A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci 86:528–534Google Scholar
  7. Banuelos GS, Ajwa HA, Mackey LL, Wu C, Cook S, Akohoue S (1997) Evaluation of different plant species used for phytoremediation of high soil selenium. J Environ Qual 26:639–646CrossRefGoogle Scholar
  8. Barcelo J, Poschenrieder C (2003) Phytoremediation: principles and perspectives. Contrib Science 2:333–344Google Scholar
  9. Barlow R, Bryant N, Andersland J, Sahi S (2000) Lead hyperaccumulation by Sesbania Drummondii. In: Proceedings of the 2000 Conference on Hazardous Waste Research, pp 112–114Google Scholar
  10. Bartoli CG, Casalongué CA, Simontacchi M, Marquez-Garcia B, Foyer CH (2013) Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environ Exp Bot 94:73–88CrossRefGoogle Scholar
  11. Baycu G (2002) Phytochelatin biosynthesis and cadmium detoxification. J Cell Mol Biol 1:45–55Google Scholar
  12. Begonia MT, Begonia GB, Ighoavodha M, Gilliard D (2005) Lead accumulation by Tall Fescue (Festuca arundinacea Schreb) grown on a lead-contaminated soil. Int J Environ Res Public Health 2:228–233PubMedPubMedCentralCrossRefGoogle Scholar
  13. Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.) Soil Biol Biochem 37:241–250CrossRefGoogle Scholar
  14. Bhatia NP, Walsh KB, Baker AJM (2005) Detection and quantification of ligands involved in nickel detoxification in a herbaceous Ni hyperaccumulator Stackhousia tryonii Bailey. J Exp Bot 56:1343–1349PubMedCrossRefGoogle Scholar
  15. Black H (1995) Absorbing possibilities: phytoremediation. Environ Health Perspect 103:1106–1108PubMedPubMedCentralCrossRefGoogle Scholar
  16. Blaylock MJ, Salt DE, Dushenkov S, Zakharova O, Gussman C, Kapulnik Y, Ensley BD, Raskin I (1997) Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agents. Environ Sci Technol 37:860–865CrossRefGoogle Scholar
  17. Bluskov S, Arocena JM (2005) Uptake, distribution, and speciation of chromium in Brassica juncea. Int J Phytoremediation 7:153–165Google Scholar
  18. Bluskov S, Arocena JM, Omotoso OO, Young JP (2005) Uptake, distribution, and speciation of chromium in Brassica juncea. Int J Phytoremediation 7:153–165Google Scholar
  19. Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends Plant Sci 3:359–362CrossRefGoogle Scholar
  20. Burken JG, Schnoor JL (1997) Uptake and metabolism of atrazine by poplar trees. Environ Sci Technol 31:1399–1406CrossRefGoogle Scholar
  21. Burken JG, Schnoor JL (1999) Distribution and volatilisation of organic compounds following uptake by hybrid poplar trees. Int J Phytoremediation 1:139–151CrossRefGoogle Scholar
  22. Chaney RL, Angle JS, McIntosh MS, Reeves RD, Li YM, Brewer EP, Chen KY, Roseberg RJ, Perner H, Synkowski EC, Broadhurst CL, Wang S, Baker AJ (2005) Using hyperaccumulator plants to phytoextract soil Ni and Cd. Z Naturforsch C 60:190–198PubMedGoogle Scholar
  23. Chen BD, Zhu YG, Smith FA (2006) Effects of arbuscular mycorrhizal inoculation on uranium and arsenic accumulation by Chinese brake fern (Pteris vittata L.) from a uranium mining-impacted soil. Chemosphere 62:1464–1473PubMedCrossRefGoogle Scholar
  24. Cheng S (2003) Effects of heavy metals on plants and resistance mechanisms. Environ Sci Pollut Res Int 10:256–264PubMedCrossRefGoogle Scholar
  25. Cobbett CS (2000) Phytochelatin biosynthesis and function in heavy-metal detoxification. Curr Opin Plant Biol 3:211–216PubMedCrossRefGoogle Scholar
  26. Cooper EM, Sims JT, Cunningham SD, Huang JW, Berti WR (1999) Chelate-assisted phytoextraction of lead from contaminated soils. J Environ Qual 28:1709–1719CrossRefGoogle Scholar
  27. Cosio C, DeSantis L, Frey B, Diallo S, Keller C (2005) Distribution of cadmium in leaves of Thlaspi caerulescens. J Exp Bot 56:765–775PubMedCrossRefGoogle Scholar
  28. Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 13:35–47CrossRefGoogle Scholar
  29. Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228CrossRefGoogle Scholar
  30. Denton B (2007) Advances in phytoremediation of heavy metals using plant growth promoting bacteria and fungi. MMG 445 Basic Biotechnol 3:1–5Google Scholar
  31. Dietz A, Schnoor JL (2001) Advances in phytoremediation. Environ Health Perspect 109:163–168PubMedPubMedCentralCrossRefGoogle Scholar
  32. Duruibe JO, Ogwuegbu MOC, Egwurugwu JN (2007) Heavy meal pollution and Human biotoxic effects. Int J Phy Sci 2:112–118Google Scholar
  33. Dushenkov V, Kumar PBAN, Motto H, Raskin I (1995) Rhirofiltration: the use of plants to remove heavy metals from aqueous streams. Environ Sci Technol 29:1239–1245PubMedCrossRefGoogle Scholar
  34. Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci 93:5624–5628. PubMedPubMedCentralCrossRefGoogle Scholar
  35. Eren E, Argüello JM (2004) Arabidopsis HMA2, a divalent heavy metal-transporting P1B-ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol 136:712–3723CrossRefGoogle Scholar
  36. Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071CrossRefGoogle Scholar
  37. Freeman JL, Michael WP, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176–2191PubMedPubMedCentralCrossRefGoogle Scholar
  38. Freeman JL, Michael WP, Nieman K, Salt DE (2005) Nickel and cobalt resistance engineered in Escherichia coli by overexpression of serine acetyltransferase from the nickel hyperaccumulator plant Thlaspi goesingense. Appl Environ Microbiol 12:8627–8633CrossRefGoogle Scholar
  39. Gardea-Torresdey JL, Rosa G, Videa JRP (2004) Use of Phytofiltration technologies in the removal of heavy metals: a review. Pure Appl Chem 76:801–813CrossRefGoogle Scholar
  40. Ghosh M, Singh SP (2005) A review on phytoremediation of heavy metals and utilization of its byproducts. Appl Ecol Environ Res 3:1–18CrossRefGoogle Scholar
  41. Giasson P, Karam A, Jaouich A (2008) Arbuscular mycorrhizae and alleviation of soil stresses on plant growth. In: Siddiqui ZA, Akhtar MS, Futai K (eds) Mycorrhizae: sustainable agriculture and forestry. Springer, Dordrecht, pp 99–134CrossRefGoogle Scholar
  42. Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. J Theor Biol 190:63–68PubMedCrossRefGoogle Scholar
  43. Gohre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122PubMedCrossRefGoogle Scholar
  44. Grcman H (2005) Phytoextraction of heavy metals from contaminated soil: expectations and limitations. Geophys Res Abstr 7:01117Google Scholar
  45. Grcman H, Vodnik D, Velikonja-Bolta S, Lestan D (2003) Ethylenediaminedisuccinate as a new chelate for environmentally safe enhanced lead phytoextraction. J Environ Qual 32:500–506PubMedCrossRefGoogle Scholar
  46. Grill E, Winnacker EL, Zenk MH (1985) Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science 230:674–676PubMedCrossRefGoogle Scholar
  47. Grill E, Loffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific y-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Nat Acad Sci U S A 86:6838–6842CrossRefGoogle Scholar
  48. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11Google Scholar
  49. Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613PubMedCrossRefGoogle Scholar
  50. Hammer DH (1986) Metallothionein. Annu Rev Biochem 55:913–951CrossRefGoogle Scholar
  51. Hammer D, Keller C (2003) Phytoextraction of Cd and Zn with Thlaspi caerulescens in field trials. Soil Use Manag 19:144–149CrossRefGoogle Scholar
  52. Hanikenne M, Kramer U, Demoulin V, Baurain D (2005) A comparative inventory of metal transporters in the green alga Chlamydomonas reinhardtii and the red alga Cyanidioschizon merolae. Plant Physiol 137:428–446PubMedPubMedCentralCrossRefGoogle Scholar
  53. Hardoim PR, Overbeek LS, Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:63–471CrossRefGoogle Scholar
  54. Hartley-Whitaker J, Ainsworth G, Vooijs R, Ten Bookum W, Schat H, Meharg AA (2001) Phytochelatins are involved in differential arsenate tolerance in Holcus lanatus. Plant Physiol 126:299–306PubMedPubMedCentralCrossRefGoogle Scholar
  55. Hossain MA, Piyatida P, Teixeira JA, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012(2):1–37. Google Scholar
  56. Huang JW, Chen J, Berti WR, Cunningham DS (1997) Phyto-remediation of lead-contaminated soils: role of synthetic chelates in lead phytoextraction. Environ Sci Technol 31:800–805CrossRefGoogle Scholar
  57. Hussain SA, Palmer DH, Moon S, Rea DW (2004) Endocrine therapy and other targeted therapies for metastatic breast cancer. Expert Rev Anticancer Ther 4:1179–1195PubMedCrossRefGoogle Scholar
  58. Ingle RA, Mugford ST, Rees JD, Campbell MM, Smith JAC (2005) Constitutively high expression of the histidine biosynthetic pathway contributes to nickel tolerance in hyperaccumulator plants. Plant Cell 17:2089–2106PubMedPubMedCentralCrossRefGoogle Scholar
  59. Jing YD, Zhen Li HE, Yang XE (2007) Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils. J Zhejiang Univ Sci B 8:192–207PubMedPubMedCentralCrossRefGoogle Scholar
  60. Jozefczak M, Keunen E, Schat H, Bliek M, Hernandez LE, Carleer R, Remans T, Bohler S, Vangronsveld J, Cuypers A (2014) Differential response of Arabidopsis leaves and roots to cadmium: glutathione-related chelating capacity vs antioxidant capacity. Plant Physiol Biochem 83:1–9PubMedCrossRefGoogle Scholar
  61. Kagi JHR (1991) Overview of metallothioneins. Methods Enzymol 205:613–626PubMedCrossRefGoogle Scholar
  62. Karthikeyan R, Kulakow PA (2003) Soil plant microbe interactions in phytoremediation. In: Phytoremediation, Advances in biochemical engineering/biotechnology, vol 78. Springer, Berlin/Heidelberg, pp 51–74CrossRefGoogle Scholar
  63. Kashem MA, Singh BR (2002) The effect of fertilizer additions on the solubility and plant–availability of Cd, Ni and Zn in soil. Nutr Cycl Agroecosyst 62:287–296CrossRefGoogle Scholar
  64. Khan FI, Husain T, Hejazi R (2004) An overview and analysis of site remediation technologies. J Environ Manag 71:95–112CrossRefGoogle Scholar
  65. Kirkham MB (2000) EDTA-facilitated phytoremediation of soil with heavy metals from sewage sludge. Int J Phytoremediation 2:159–172CrossRefGoogle Scholar
  66. Kruszka K, Pieczynski M, Windels D, Bielewicz D, Jarmolowski A, Szweykowska-Kulinska Z, Vazquez F (2012) Role of microRNAs and other sRNAs of plants in their changing environments. J Plant Physiol 169:1664–1672PubMedCrossRefGoogle Scholar
  67. Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant-Microbe Interact 17:6–15PubMedCrossRefGoogle Scholar
  68. Kuklinsky-Sobral J, Araujo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251PubMedCrossRefGoogle Scholar
  69. Kupper H, Lombi E, Zhao FJ, Wieshammer G, McGrath SP (2001) Cellular Compartmentation of Ni in the hyperaccumulators Alyssum lesbiacum, A. bertolonii and Thlaspi goesingense. J Exp Bot 52:2291–2300PubMedCrossRefGoogle Scholar
  70. Lasat MM (2002) Phytoextraction of toxic metals. A review of biological mechanisms. J Environ Qual 31:109–120PubMedCrossRefGoogle Scholar
  71. Lee S, Moon JS, Ko TS, Petros D, Goldsbrough PB, Korban SS (2003) Over expression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiol 131:656–663PubMedPubMedCentralCrossRefGoogle Scholar
  72. Lee M, Lee K, Lee J, Noh EW, Lee Y (2005) AtPDR12 Contributes to lead resistance in Arabidopsis. Plant Physiol 138:827–836PubMedPubMedCentralCrossRefGoogle Scholar
  73. Liphadzi MS, Kirkham MB (2005) Phytoremediation of soil contaminated with heavy metals: a technology for rehabilitation of the environment. J S Afr Bot 71:24–37CrossRefGoogle Scholar
  74. Lone MI, He Z, Stoffella PJ, Yang X (2008) Phytoremediation of heavy metal polluted soils and water: progress and perspectives. J Zhejiang UniSci B 9:210–220CrossRefGoogle Scholar
  75. Madrid F, Liphadzi MS, Kirkham MB (2003) Heavy metal displacement in chelate-irrigated soil during phytoremediation. J Hydrol 272:107–119CrossRefGoogle Scholar
  76. Manara A (2012) Plant responses to heavy metal toxicity. In: Plants and heavy metals, pp 27–54. CrossRefGoogle Scholar
  77. McGrath SP (1998) Phytoextraction for soil remediation. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CABI Publishing, Wallingford, pp 261–287Google Scholar
  78. Memon A, Aktoprakligil D, Ozdemir Z, Vertii A (2001) Heavy metal accumulation and detoxification mechanism in plants. Turk J Bot 25:111–121Google Scholar
  79. Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum. I. J Exp Bot 56:167–178Google Scholar
  80. Miller RR (1996) Phytoremediation, technology overview report, Ground-water remediation technologies analysis center, Pittsburgh, PA, USA web.
  81. Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13PubMedPubMedCentralCrossRefGoogle Scholar
  82. Mukhopadhyay S, Maiti SK (2010) Phytoremediation of metal enriched mine waste: a review. Global J Environ Res 4:135–150Google Scholar
  83. Nascimento CWA, Xing B (2006) Phytoexraction: a review on enhanced metal availability and plant accumulation. Sci Agric 63:299–311CrossRefGoogle Scholar
  84. Nedkovska M, Atanassov AI (1998) Metallothionein genes and expression for heavy metal resistance. Biotechnology 12:11–16Google Scholar
  85. Nguyen VNT, Moon S, Jung K-H (2014) Genome-wide expression analysis of rice ABC transporter family across spatio-temporal samples and in response to abiotic stresses. J Plant Physiol 171:1276–1288PubMedCrossRefGoogle Scholar
  86. Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484PubMedCrossRefGoogle Scholar
  87. Ortiz DF, Theresa R, McCue KF, Ow DW (1995) Transport of metal -binding peptides by HMT1, A Fission yeast ABC-type Vacuolar Membrane Protein. J Biol Chem 270(9):4721–4728Google Scholar
  88. Ovečka M, Takáč T (2014) Managing heavy metal toxicity stress in plants: biological and biotechnological tools. Biotechnol Adv 32:73–86PubMedCrossRefGoogle Scholar
  89. Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyperaccumulation metals in plants. Water Air Soil Pollut 184:105–126Google Scholar
  90. Panda SK (2003) Heavy metal toxicity induces oxidative stress in a moss Taxithellium sp. Curr Sci 84:631–633Google Scholar
  91. Papoyan A, Kochian LV (2004) Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol 136:3814–3823PubMedPubMedCentralCrossRefGoogle Scholar
  92. Pence NS, Larsen PB, Ebbs SD, Letham DLD, Lasat MM, Garvin DF, Eid D, Kochian LV (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci U S A 97:4956–4960PubMedPubMedCentralCrossRefGoogle Scholar
  93. Persans MW, Yan X, Patnoe JMML, Krämer U, Salt DE (1999) Molecular dissection of the role of histidine in nickel hyperaccumulation in Thlaspi goesingense (Hálácsy). Plant Physiol 121:1117–1126PubMedPubMedCentralCrossRefGoogle Scholar
  94. Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39PubMedCrossRefGoogle Scholar
  95. Pivetz BE (2001) Phytoremediation of contaminated soil and ground water at hazardous sites. Ground water issue, EPA/540/S-01/500Google Scholar
  96. Plaza S, Tearall KL, Zhao FJ, Buchner P, McGrath SP, Hawkesford MJ (2007) Expression and functional analysis of metal transporter genes in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 58:1717–1728PubMedCrossRefGoogle Scholar
  97. Prasad MNV, Freitas HM (2003) Metal hyperaccumulation in plants–biodiversity prospecting for phytoremediation technology. Electron J Biotechnol 6:285–321CrossRefGoogle Scholar
  98. Rafati M, Khorasani N, Moattar F, Shirvany A, Moraghebi F, Hosseinzadeh S (2011) Phytoremediation potential of Populus alba and Morus alba for cadmium, chromium and nickel absorption from polluted soil. Int J Environ Res 5:961–970Google Scholar
  99. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore producing bacteria for improving heavy metal phytoextraction. Trends Microbiol 28:142–149Google Scholar
  100. Robinson NJ, Tommey AM, Kuske C, Jackson PJ (1993) Plant metallothioneins. J Biochem 295:1–10CrossRefGoogle Scholar
  101. Robinson B, Schulin R, Nowack B, Roulier S, Menon M, Clothier B, Green S, Mills T (2006) Phytoremediation for the management of metal flux in contaminated sites. For Snow Landsc Res 80:221–234Google Scholar
  102. Ross S (1994) Toxic metals in soil-plant systems. Wiley, Chichester. ISBN: 978-0-471-94279-5Google Scholar
  103. Ruby MV, Schoff R, Battin W, Goldade M, Post G, Harnois M, Mosby DE, Casteel SW, Berti W, Carpenter M, Edwards D, Cargin D, Chappel W (1999) Advances in evaluating the oral bioavailability of inorganics in soil for use in human health risk assessment. Environ Sci Technol 32:3697–3705CrossRefGoogle Scholar
  104. Salt DE, Wagner GJ (1993) Cadmium transport across tonoplast of vesicles from oat roots evidence for a Cd2+/H+ antiport acivity. J Biol Chem 268:12297–12302PubMedGoogle Scholar
  105. Sawidis T (2008) Effect of cadmium on pollen germination and tube growth in Lilium longiflorum and Nicotiana tabacum. Protoplasma 233:95–106PubMedCrossRefGoogle Scholar
  106. Sewelam N, Jaspert N, Van Der Kelen K, Tognetti VB, Schmitz J, Frerigmann H, Stahl E, Zeier J, Van Breusegem F, Maurino VG (2014) Spatial H2O2 signaling specificity: H2O2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially. Mol Plant 7:1191–1210PubMedCrossRefGoogle Scholar
  107. 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 57:711–726PubMedCrossRefGoogle Scholar
  108. Siciliano SD, Germida JJ (1998) Mechanisms of phytoremediation: biochemical and ecological interactions between plants and bacteria. Environ Rev 6:65–79CrossRefGoogle Scholar
  109. Srivastava M, Ma LQ, Singh N, Singh S (2005) Antioxidant responses of hyper-accumulator and sensitive fern species to arsenic. J Exp Bot 56:1335–1342PubMedCrossRefGoogle Scholar
  110. Stanhope KG, Young SD, Hutchinson JJ, Kamath R (2000) Use of isotopic dilution techniques to assess the mobilization of nonliable Cd by chelating agents in phytoremediation. Environ Sci Technol 34:4123–4127CrossRefGoogle Scholar
  111. Ste’phane M, Gendre D, Pianelli K, Ouerdane L, Lobinski R, Briat JF, Lebrun M, Czernic P (2006) Root-to-shoot long-distance circulation of nicotianamine and nicotianamine–nickel chelates in the metal hyperaccumulator Thlaspi caerulescens. J Exp Bot 57:4111–4122CrossRefGoogle Scholar
  112. Sudhakar G, Jyothi B, Venkateshwar V (1991) Metal pollution and its impact on algae in flowing waters in India. Arch Environ Contam Toxicol 21:556–266PubMedCrossRefGoogle Scholar
  113. Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci U S A 97:4991–4996PubMedPubMedCentralCrossRefGoogle Scholar
  114. Triplett EW (1996) Diazotrophic endophytes: progress and prospects for nitrogen fixation in monocots. Plant Soil 186:2938CrossRefGoogle Scholar
  115. Ueno D, Iwashita T, Zhao FJ, Ma JF (2008) Characterization of Cd Translocation and Identification of the Cd Form in Xylem Sap of the Cd-Hyperaccumulator Arabidopsis halleri. Plant Cell Physiol 49:540–548PubMedCrossRefGoogle Scholar
  116. US DOE (1994) Summary report of a workshop on phytoremediation research needs. In: Benemann JR, Rabson R, Travares J, Levine R (eds), Santa Rosa, CA July 24–26, 1994. Report DOE/EM-0224, US DOE, December 1994, Washington, DCGoogle Scholar
  117. USEPA (1999) Report on bioavailability of chemical wastes with respect to the potential for soil remediation. T28006: QT-DC-99-003260Google Scholar
  118. USEPA (2000) Introduction to phytoremediation. Cincinnati OH, US EPA: 104Google Scholar
  119. Variyar PS, Banerjee A, Akkarakaran JJ, Suprasanna P (2014) Role of glucosinolates in plant stress tolerance. In: Emerging technologies and management of crop stress tolerance. Academic, San Diego, pp 271–291CrossRefGoogle Scholar
  120. Vatamaniuk OK, Bucher EA, Sundaram MV, Rea PA (2005) CeHMT-1, a putative phytochelatin transporter, is required for cadmium tolerance in Caenorhabditis elegans. J Biol Chem 280:23684–23690PubMedCrossRefGoogle Scholar
  121. Violante A, Cozzolino V, Perelomov L, Caporale AG, Pigna M (2010) Mobility and bioavailability of heavy metals and metalloids in soil environments. J Soil Sci Plant Nutr 10:268–292CrossRefGoogle Scholar
  122. Visioli G, Marmiroli N (2012) The proteomics of heavy metal hyperaccumulation by plants. J Proteome 79:133–145CrossRefGoogle Scholar
  123. Wase J, Forster C (1997) Biosorbents for metal ions. Taylor and Francis Ltd, LondonGoogle Scholar
  124. Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: Plant-endophyte partnerships take the challenge. Curr Opin Biotechnol 20:1–7CrossRefGoogle Scholar
  125. Wong JWC, Wong WWY, Wei Z, Jagadeesan H (2004) Alkaline biosolids and EDTA for phytoremediation of an acidic loamy soil spiked with cadmium. Sci Total Environ 24:235–246CrossRefGoogle Scholar
  126. Wu J, Hsu FC, Cunningham SD (1999) Chelate-assisted Pb phytoextraction: Pb availability, uptake, and translocation constraints. Environ Sci Technol 33:1898–1904CrossRefGoogle Scholar
  127. Yan JW, Zhang LY (2013) Molecular cloning and characterization of a Brassica juncea yellow stripe-like gene, BjYSL7, whose overexpression increases heavy metal tolerance of tobacco. Plant Cell Rep 32(5):651–662CrossRefGoogle Scholar
  128. Yong SW, Martinoia E, Lee J, Kim D, Kim DY, Vogt E, Shim D, Choi KS, Hwang I, Lee Y (2004) A novel family of cys-rich membrane proteins mediates cadmium resistance in Arabidopsis. Plant Physiol 135:1027–1039CrossRefGoogle Scholar
  129. Yoon J, Cao X, Zhou Q, Ma LQ (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464PubMedCrossRefGoogle Scholar
  130. Yuan J, Chen D, Ren Y, Zhang X, Zhao J (2008) Characteristic and expression analysis of a metallothionein gene, OsMT2b, down-regulated by cytokinin suggests functions in root development and seed embryo germination of rice. Plant Physiol 146:1637–1650PubMedPubMedCentralCrossRefGoogle Scholar
  131. Zacchini M, Pietrini F, Mugnozza GS, Iori V, Pietrosanti L, Massacci A (2009) Metal tolerance, accumulation and translocation in poplar and willow clones treated with cadmium in hydroponics. Water Air Soil Pollut 197:23–34CrossRefGoogle Scholar
  132. Zenk MH (1996) Heavy metal detoxification in higher plants–a review. Gene 179:21–30PubMedCrossRefGoogle Scholar
  133. Zhu YG, Kneer R, Tong YP (2004) Vacuolar compartmentalization: a second-generation approach to engineering plants for phytoremediation. Trends Plant Sci 9:7–9PubMedGoogle Scholar
  134. Zhuang P, Yang Q, Wang H, Shu W (2007) Phytoextraction of heavy metals by eight plant species in the field. Water Air Soil Pollut 184:235–242CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Smita S. Kumar
    • 1
  • Abudukeremu Kadier
    • 2
  • Sandeep K. Malyan
    • 3
  • Altaf Ahmad
    • 4
  • Narsi R. Bishnoi
    • 1
    Email author
  1. 1.Department of Environmental Science and EngineeringGuru Jambheshwar University of Science and TechnologyHisarIndia
  2. 2.Department of Chemical and Process Engineering, Faculty of Engineering and Built EnvironmentNational University of Malaysia (UKM)UKM BangiMalaysia
  3. 3.Centre for Environment Science and Climate Resilient AgricultureICAR-Indian Agricultural Research InstituteNew DelhiIndia
  4. 4.Department of BotanyAligarh Muslim UniversityAligarhIndia

Personalised recommendations