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Heavy Metal Hyperaccumulation and Hypertolerance in Brassicaceae

  • Mudasir Irfan Dar
  • Mohd Irfan Naikoo
  • Iain D. Green
  • Nusrath Sayeed
  • Barkat Ali
  • Fareed Ahmad Khan
Chapter

Abstract

Several members of Brassicaceae family are well known metal accumulators. High metal translocation from their roots to above ground shoots without showing any phytotoxic symptoms make them potential candidates for remediation of various metal/metalloid contaminated areas. These plants tolerate the high amount of accumulated heavy metals by sequestering them into vacuoles of aboveground parts especially leaves. This is partly done by overexpression of specific metal transporters in different tissues from metal uptake in the root and shoot up to the storage sites (non sensitive) in the leaf. Hyperaccumulation and hypertolerance traits associated with Brassicaceae ignited interests in scientific community to understand and investigate the range of mechanisms and omics in these plants with relation to accumulation of metals and their detoxification. In this chapter we will try to discuss the mechanism of heavy metal uptake in Brassicaceae and their tolerance and detoxification pathways in these plants.

Keywords

Brassicaceae Heavy metal Hyperaccumulation Uptake Detoxification 

References

  1. Alkorta I, Hernandez-Allica J, Becerril JM, Amezaga I, Albizu I, Garbisu C (2004) Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead, and arsenic. Rev Environ Sci Biotechnol 3:71–90CrossRefGoogle Scholar
  2. Anjum NA, Ahmad I, Pereira ME, Duarte AC, Umar S, Khan NA (2012) The plant family brassicaceae: an introduction. In: Anjum NA, Ahmad I, Pereira ME, Duarte AC, Umar S, Khan NA (eds) The plant family Brassicaceae: contribution towards phytoremediation. Springer, Dordrecht, pp 1–33CrossRefGoogle Scholar
  3. Asemaneh T, Ghaderian SM, Crawford SA, Marshall AT, Baker AJM (2006) Cellular and subcellular compartmentation of Ni in the Eurasian serpentine plants Alyssum bracteatum, Alyssum murale (Brassicaceae) and Cleome heratensis (Capparaceae). Planta 225:193–290PubMedCrossRefPubMedCentralGoogle Scholar
  4. Assuncao AGL, da Costa MP, de Folter S, Voojis R, Schat H, Aarts MGM (2001) Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 24:217–226CrossRefGoogle Scholar
  5. Assuncao AGL, Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419CrossRefGoogle Scholar
  6. Assuncao AGL, Bleeker P, Ten Bookum WM, Vooijs R, Schat H (2008) Intraspecific variation of metal preference patterns for hyperaccumulation in Thlaspi caerulescens: evidence for binary metal exposures. Plant Soil 303:289–299CrossRefGoogle Scholar
  7. Assuncao AGL, Herrero E, Lin Y-F, Huettel B, Talukdar S, Smaczniak C, Immink RGH, van Eldik M, Fiers M, Schat H, Aarts MGM (2010) Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency. Proc Natl Acad Sci U S A 107:10296–10301PubMedPubMedCentralCrossRefGoogle Scholar
  8. Axelsen KB, Palmgren MG (1998) Inventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiol 126:696–706CrossRefGoogle Scholar
  9. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements - a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126Google Scholar
  10. Baker AJM, Whiting SN (2002) In search of the holy grail – a further step in understanding metal hyperaccumulation? New Phytol 155:1–7CrossRefGoogle Scholar
  11. Baker AJM, McGrath SP, Reeves DR, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, pp 85–107Google Scholar
  12. Basic N, Keller C, Fontanillas P, Besnard G, Galland N (2006) Cadmium hyperaccumulation and reproductive traits in natural Thlaspi caerulescens populations. Plant Biol 8:64–72PubMedCrossRefGoogle Scholar
  13. Bidwell SD, Crawford SA, Woodrow IE, Sommer-Knudsen J, Marshall AT (2004) Sub-cellular localization of Ni in the hyperaccumulator, Hybanthus floribundus (Lindley) F. Muell. Plant Cell Environ 27:705–716CrossRefGoogle Scholar
  14. Brooks RR (1998) Biogeochemistry and hyperaccumulators. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB International, Wallingford, pp 95–118Google Scholar
  15. Callahan DL, Baker AJM, Kolev SD, Wedd AG (2006) Metal ion ligands in hyperaccumulating plants. J Biol Inorg Chem 11:2–12PubMedCrossRefGoogle Scholar
  16. Chaffai R, Koyama H (2011) Heavy metal tolerance in Arabidopsis thaliana. Adv Bot Res 60:1–49CrossRefGoogle Scholar
  17. Chiang HC, Lo J-C, Yeh K-C (2006) Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environ Sci Technol 40:6792–6798PubMedCrossRefGoogle Scholar
  18. Cho-Ruk K, Kurukote J, Supprung P, Vetayasuporn S (2006) Perennial plants in the phytoremediation of lead contaminated soils. Biotechnology 5:1–4CrossRefGoogle Scholar
  19. Colangelo EP, Guerinot ML (2006) Put the metal to the petal: metal uptake and transport throughout plants. Curr Opin Plant Biol 9:322–330PubMedCrossRefGoogle Scholar
  20. Craciun AR, Courbot M, Bourgis F, Salis P, Saumitou-Laprade P, Verbruggen N (2006) Comparative cDNA-AFLP analysis of Cd-tolerant and – sensitive genotypes derived from crosses between the Cd hyperaccumulator Arabidopsis halleri and Arabidopsis lyrata spp. Petraea. J Exp Bot 57:2967–2983PubMedCrossRefGoogle Scholar
  21. Dar MI, Khan FA, Green ID, Naikoo MI (2015a) The transfer and fate of Pb from sewage sludge amended soil in a multi-trophic food chain: a comparison with the labile elements Cd and Zn. Environ Sci Pollut Res 22:16133–16142CrossRefGoogle Scholar
  22. Dar MI, Khan FA, Rehman F, Masoodi A, Ansari AA, Varshney D, Naushin F, Naikoo MI (2015b) Roles of Brassicaceae in phytoremediation of metals and metalloids. In: Ansari AA, Gill SS, Lanza GR, Newman L (eds) Phytoremediation: management of environmental contaminants. Springer, Cham, pp 201–215Google Scholar
  23. Dar MI, Green ID, Naikoo MI, Khan FA, Ansari AA, Lone MI (2017) Assessment of biotransfer and bioaccumulation of cadmium, lead and zinc from fly ash amended soil in mustard-aphid-beetle food chain. Sci Total Environ 584:1221–1229PubMedCrossRefGoogle Scholar
  24. Delorme TA, Gagliardi JV, Angle JS, Chaney RL (2001) Influence of the zinc hyperaccumulator Thlaspi caerulescens J. and C. Presl. and the non-metal accumulator Trifolium pratense L. on soil microbial populations. Can J Microbiol 47:773–776PubMedCrossRefGoogle Scholar
  25. Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205PubMedPubMedCentralCrossRefGoogle Scholar
  26. Erakhrumen A, Agbontalor A (2007) Phytoremediation: an environmentally sound technology for pollution prevention, control and remediation in developing countries. Educ Res Rev 2:151–156Google Scholar
  27. Gendre D, Czernic P, Conejero G, Pianelli K, Briat J-F, Lebrum M, Mari S (2007) TcYSL3, a member of the YSL gene family from the hyperaccumulator Thlaspi caerulescens, encodes a nicotinamine–Ni/Fe transporter. Plant J 49:1–15PubMedCrossRefGoogle Scholar
  28. Ghasemi R, Ghaderian SM, Kramer U (2009) Accumulation of nickel in trichomes of a nickel hyperaccumulator plant, Alyssum inflatum. North East Nat 16:81–92CrossRefGoogle Scholar
  29. Gustin JL, Loureiro ME, Kim D, Na G, Tikhonova M, Salt DE (2009) MTP1-dependent Zn sequestration into shoot vacuoles suggests dual roles in Zn tolerance and accumulation in Zn hyperaccumulating plants. Plant J 57:1116–1127PubMedCrossRefGoogle Scholar
  30. Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Kramer U (2008) Evolution of metal hyperaccumulation required cis regulatory changes and triplication of HMA4. Nature 453:391–395PubMedCrossRefPubMedCentralGoogle Scholar
  31. Hassan Z, Aarts MGM (2010) Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environ Exp Bot 72:53–63CrossRefGoogle Scholar
  32. Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506PubMedCrossRefPubMedCentralGoogle Scholar
  33. Hinchman RR, Negri CM, Gatliff EG (1996) Phytoremediation: using green plants to clean up contaminated soil, groundwater and wastewater. Proc Int Top Meet Nucl Hazard Waste Manag Spectr 96:1–13Google Scholar
  34. 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
  35. Jabeen R, Ahmad A, Iqbal M (2009) Phytoremediation of heavy metals: physiological and molecular mechanisms. Bot Rev 75:339–364CrossRefGoogle Scholar
  36. Kerkeb L, Kramer U (2003) The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiol 131:716–724PubMedPubMedCentralCrossRefGoogle Scholar
  37. Kim D, Gustin JL, Lahner B, Persans MW, Baek D, Yun DJ, Salt DE (2004) The plant CDF family member TgMTP1 from the Ni/Zn hyperaccumulator Thlaspi goesingense acts to enhance efflux of Zn at the plasma membrane when expressed in Saccharomyces cerevisiae. Plant J 39:237–251PubMedCrossRefPubMedCentralGoogle Scholar
  38. Kramer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534PubMedCrossRefPubMedCentralGoogle Scholar
  39. Kramer U, Smith RD, Wenzel WW, Raskin I, Salt DE (1997) The role of metal transport and tolerance in nickel hyperaccumulation by Thlaspi goesingense Halacsy. Physiol Plant 115:1641–1650CrossRefGoogle Scholar
  40. Kramer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol 122:1343–1354PubMedPubMedCentralCrossRefGoogle Scholar
  41. Kramer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272PubMedCrossRefPubMedCentralGoogle Scholar
  42. Kubota H, Takenaka C (2003) Arabis gemmifera is a hyperaccumulator of Cd and Zn. Int J Phytoremediation 5:197–201PubMedCrossRefPubMedCentralGoogle Scholar
  43. Kumar PBAN, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238PubMedCrossRefPubMedCentralGoogle Scholar
  44. Kupper H, Kochian LV (2010) Transcriptional regulation of metal transport genes and mineral nutrition during acclimatization to cadmium and zinc in the Cd/Zn hyperaccumulator, Thlaspi caerulescens (Ganges population). New Phytol 185:114–129PubMedCrossRefPubMedCentralGoogle Scholar
  45. Kupper H, Zhao FJ, McGrath SP (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119:305–311PubMedCentralCrossRefGoogle Scholar
  46. Kupper H, Lombi E, Zhao FJ, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212:75–84PubMedCrossRefPubMedCentralGoogle Scholar
  47. Kupper H, Lombi E, Zhao FJ, Wieshammer G, McGrath SP (2001) Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J Exp Bot 52:2291–2300PubMedCrossRefPubMedCentralGoogle Scholar
  48. Lasat MM, Baker AJM, Kochian LV (1998) Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in hyperaccumulation in Thlaspi caerulescens. Plant Physiol 118:875–883PubMedPubMedCentralCrossRefGoogle Scholar
  49. Lasat MM, Pence NS, Garvin DF, Abbs SD, Kochian LV (2000) Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. J Exp Bot 51:71–79PubMedCrossRefPubMedCentralGoogle Scholar
  50. Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytol 145:11–20CrossRefGoogle Scholar
  51. Lombi E, Zhao FJ, McGrath SP, Young SD, Sacchi GA (2001) Physiological evidence for a high-affinity cadmium transporter highly expressed in a Thlaspi caerulescens ecotype. New Phytol 149:53–60CrossRefGoogle Scholar
  52. Lombi E, Tearall KL, Howarth JR, Zhao FJ, Hawkesford MJ, McGrath SP (2002) Influence of iron status on cadmium and zinc uptake by different ecotypes of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 128:1359–1367PubMedPubMedCentralCrossRefGoogle Scholar
  53. Ma JF, Ueno D, Zhao FJ, McGrath SP (2005) Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 220:731–736PubMedCrossRefGoogle Scholar
  54. Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: cost and trade-offs between traits and environment. Environ Exp Bot 68:1–13CrossRefGoogle Scholar
  55. Mellem JJ, Baijnath H, Odhav B (2012) Bioaccumulation of Cr, Hg, As, Pb, Cu and Ni with the ability for hyperaccumulation by Amaranthus dubius. Afr J Agric Res 7:591–596Google Scholar
  56. Mills RF, Krijger GC, Baccarini PJ, Hall JL, Williams LE (2003) Functional expression of AtHMA4, a P1B-type ATPase of the Zn/Co/Cd/Pb subclass. Plant J 35:164–176PubMedCrossRefGoogle Scholar
  57. Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13PubMedPubMedCentralCrossRefGoogle Scholar
  58. Neilson S, Rajakaruna N (2012) Roles of rhizospheric processes and plant physiology in phytoremediation of contaminated sites using oilseed Brassicas. In: Anjum NA, Ahmad I, Pereira ME, Duarte AC, Umar S, Khan NA (eds) The plant family Brassicaceae: contribution towards phytoremediation. Springer, Dordrecht, pp 313–330CrossRefGoogle Scholar
  59. Palmer CE, Warwick S, Keller W (2001) Brassicaceae (Cruciferae) family, plant biotechnology, and phytoremediation. Int J Phytoremediation 3:245–287CrossRefGoogle Scholar
  60. 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
  61. Peiter E, Montanini B, Gobert A, Pedas P, Husted S, Maathuis FJM, Blaudez D, Chalot M, Sanders D (2007) A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance. Proc Natl Acad Sci U S A 104:8532–8537PubMedPubMedCentralCrossRefGoogle Scholar
  62. Pence NS, Larsen PB, Ebbs SD, Letham DBL, Lasat MM, Garvin DF, Eide 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
  63. Persant MW, Nieman K, Salt DE (2001) Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Plant Biol 98:9995–10000Google Scholar
  64. Prasad MNV (2005) Nickelophilous plants and their significance in phytotechnologies. Braz J Plant Physiol 17:113–128CrossRefGoogle Scholar
  65. Prasad MNV, Freitas HMO (2003) Metal hyperaccumulation in plants- biodiversity prospecting for phytoremediation technology. Electron J Biotechnol 6:285–321CrossRefGoogle Scholar
  66. Puschenreiter M, Wieczorek S, Horak O, Wenzel WW (2003) Chemical changes in the rhizosphere of metal hyperaccumulator excluder Thalspi species. J Plant Nutr Soil Sci 168:579–584CrossRefGoogle Scholar
  67. Raab A, Feldman J, Meharg AA (2004) The nature of arsenic–phytochelatins complexes in Holcus lanatus and Pteris cretica. Plant Physiol 134:1113–1122PubMedPubMedCentralCrossRefGoogle Scholar
  68. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? and what makes them so interesting? Plant Sci 180:69–181CrossRefGoogle Scholar
  69. Reeves RD, Baker AJM, Borhidi A, Berazain R (1999) Nickel hyperaccumulation in the serpentine flora of Cuba. Ann Bot 83:29–38CrossRefGoogle Scholar
  70. Robinson BH, Lombi E, Zhao FJ, McGrath SP (2003) Uptake and distribution of nickel and other metals in the hyperaccumulator Berkheya coddii. New Phytol 158:279–285CrossRefGoogle Scholar
  71. Roosens N, Verbruggen N, Meerts P, Ximenez-Embun P, Smith JAC (2003) Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from Western Europe. Plant Cell Environ 26:1657–1672CrossRefGoogle Scholar
  72. Roosens NH, Bernard C, Leplae R, Verbruggen N (2004) Evidence for copper homeostasis function of metallothionein (MT3) in the hyperaccumulator Thlaspi caerulescens. FEBS Lett 577:9–16PubMedCrossRefPubMedCentralGoogle Scholar
  73. Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433PubMedPubMedCentralCrossRefGoogle Scholar
  74. Salt DE, Prince RC, Baker AJM, Raskin I, Pickering IJ (1999) Zinc ligand in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environ Sci Technol 33:713–717CrossRefGoogle Scholar
  75. Sarma H (2011) Metal hyperaccumulation in plants: a review focussing on phytoremediation technology. Environ Sci Technol 4:118–138CrossRefGoogle Scholar
  76. Sarret G, Saumitou-Laprade P, Bert V, Proux O, Hazemann JL, Traverse A, Marcus MA, Manceau A (2002) Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiol 130:1815–1826PubMedPubMedCentralCrossRefGoogle Scholar
  77. Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T, Davies JP (2002) Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J 29:475–486PubMedCrossRefPubMedCentralGoogle Scholar
  78. Sors TG, Ellis DR, Salt DE (2005) Selenium uptake, translocation, assimilation and metabolic fate in plants. Photosynth Res 86:373–389PubMedCrossRefPubMedCentralGoogle Scholar
  79. Sors TG, Martin CP, Salt DE (2009) Characterization of selenocysteine methyltransferases from Astragalus species with contrasting selenium accumulation capacity. Plant J 59:110–122PubMedCrossRefPubMedCentralGoogle Scholar
  80. Stephan UW, Scholz G (1993) Nicotianamine: mediator of transport of iron and heavy metals in the phloem? Physiol Plant 88:522–529CrossRefGoogle Scholar
  81. Talke IN, Hanikenne M, Kramer U (2006) Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 142:148–167PubMedPubMedCentralCrossRefGoogle Scholar
  82. Tang Y-T, Qiu R-L, Zeng X-W, Ying R-R, Yu F-M, Zhou X-Y (2009) Lead, Zinc, Cadmium accumulation and growth simulation in Arabis paniculata. Franch. Environ Exp Bot 66:126–134CrossRefGoogle Scholar
  83. Tangahu BV, Abdullah SRS, Basri H, Idris M, Anuar N, Mukhlisin M (2011) A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. Int J Chem Eng 939161:1–31CrossRefGoogle Scholar
  84. Thakur S, Singh L, Wahid ZA, Siddiqui MF, Atnaw SM, Din MFM (2016) Plant-driven removal of heavy metals from soil: uptake, translocation, tolerance mechanism, challenges, and future perspectives. Environ Monit Assess 188:206.  https://doi.org/10.1007/s10661-016-5211-9 CrossRefPubMedPubMedCentralGoogle Scholar
  85. van de Mortel JE, Schat H, Moerland PD, Ver Loren van Themaat E, van der Ent S, Blankestijn H, Ghandilyan A, Tsiatsiani S, Aarts MG (2008) Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 31:301–324PubMedCrossRefPubMedCentralGoogle Scholar
  86. Vazquez MD, Poschenrieder C, Barcelo J, Baker AJM, Hatton P, Cope GH (1994) Compartmentation of zinc in roots and leaves of the zinc hyperaccumulator Thlaspi caerulescens J & C Presl. Bot Acta 107:243–250CrossRefGoogle Scholar
  87. Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776PubMedCrossRefPubMedCentralGoogle Scholar
  88. Vogel-Mikus K, Drobne D, Regvar M (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine. Environ Pollut 133:233–242PubMedCrossRefPubMedCentralGoogle Scholar
  89. Vogel-Mikus K, Simcic J, Pelicon P, Budnar M, Kump P, Necemer M, Mesjasz-Przybyłowicz J, Przybyłowicz WJ, Regvar M (2008) Comparison of essential and non-essential element distribution in leaves of the Cd/Zn hyperaccumulator Thlaspi praecox as revealed by micro-PIXE. Plant Cell Environ 31:1484–1496PubMedCrossRefPubMedCentralGoogle Scholar
  90. Weber M, Harada E, Vess C, Roepenack-Lahaye E, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281PubMedCrossRefGoogle Scholar
  91. Wycisk K, Kimb EJ, Schroeder JI, Kramer U (2004) Enhancing the first enzymatic step in the histidine biosynthesis pathway increases the free histidine pool and nickel tolerance in Arabidopsis thaliana. FEBS Lett 578:128–134PubMedCrossRefGoogle Scholar
  92. Yang XE, Long XX, Ye HB, He ZL, Calvert DV, Stoffella PJ (2004) Cadmium tolerance and hyperaccumulation in a new Zn hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259:181–189CrossRefGoogle Scholar
  93. Zhao FJ, Lombi E, Breedon T, McGrath SP (2000) Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ 23:507–514CrossRefGoogle Scholar
  94. Zhao FJ, Dunham SJ, McGrath SP (2002a) Arsenic hyperaccumulation by different fern species. New Phytol 156:27–31CrossRefGoogle Scholar
  95. Zhao FJ, Hamon RE, Lombi E, McLaughlin MJ, McGrath SP (2002b) Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 53:535–543PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Mudasir Irfan Dar
    • 1
  • Mohd Irfan Naikoo
    • 2
  • Iain D. Green
    • 3
  • Nusrath Sayeed
    • 1
  • Barkat Ali
    • 1
  • Fareed Ahmad Khan
    • 2
  1. 1.Department of BotanyGovernment College for WomenSrinagarIndia
  2. 2.Environmental Botany Section, Department of BotanyAligarh Muslim UniversityAligarhIndia
  3. 3.Department of Life and Environmental Science, The Faculty of Science and TechnologyBournemouth UniversityDorsetUK

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