Skip to main content
SpringerLink
Log in

Engineered Plants for Heavy Metals and Metalloids Tolerance

  • Chapter
  • First Online:
Genetic Manipulation in Plants for Mitigation of Climate Change

Abstract

Agricultural soils around the world are slightly to moderately polluted with heavy metals such as As, Cd, Hg, Cr, Cu, Pb, Ni, and Zn as a result of industrialization, widespread application of pesticides, fertilizers, and anthropogenic activities. Plants experience toxic effects of heavy metals in the form of oxidative stress, reduction in overall growth, and productivity. To minimize these toxic effects, plants have evolved an arsenal of mechanisms such as preventing uptake via roots or blocking transport to aboveground parts. If everything fails, the toxic metal inside the cell is dealt with using a range of detoxification and storage strategies including chelation with thiols and amino acids and subsequent sequestration into subcellular compartments. In this chapter, we have reviewed general strategies for heavy metal tolerance and detoxification by plants. Also plants engineered for heavy metal transport, oxidative stress tolerance pathways, and other mechanisms such as stress-associated protein have substantially advanced our understanding of heavy metal tolerance by plants. In future, as a result of ongoing climate change, frequent floods, storms, and more use of underground and recycled water from industrial and municipal wastes for crop irrigation can further increase the heavy metals in the agricultural soils. Therefore, to minimize the impact of heavy metals on global agricultural production, it will be of utmost importance to further our knowledge of heavy metal tolerance and detoxification by plants.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abedin MJ, Feldmann J, Meharg AA (2002) Uptake kinetics of arsenic species in rice plants. Plant Physiol 128:1120–1128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson JW (1993) Selenium interactions in sulfur metabolism. In: De Kok LJ (ed) Sulfur nutrition and assimilation in higher plants-regulatory, agricultural and environmental aspects. SPB Academic Publishing, The Hague, pp 49–60

    Google Scholar 

  • Arazi T, Sunkar R, Kaplan B, Fromm H (1999) A tobacco plasma membrane calmodulin-binding transporter confers Ni2+ tolerance and Pb2+ hypersensitivity in transgenic plants. Plant J 20:171–182

    Article  CAS  PubMed  Google Scholar 

  • Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206

    Article  Google Scholar 

  • Auguy F, Fahr M, Moulin P, Brugel A, Laplaze L, El Mzibri M, Filali-Maltouf A, Doumas P, Smouni A (2013) Lead tolerance and accumulation in Hirschfeldia incana, a Mediterranean Brassicaceae from metalliferous mine spoils. PLoS One 8:e61932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aust SD, Morehouse LA, Thomas CE (1985) Role of metals in oxygen radical reactions. J Free Radic Biol Med 1:3–25

    Article  CAS  PubMed  Google Scholar 

  • Balogh SJ, Swain EB, Nollet YH (2006) Elevated methylmercury concentrations and loadings during flooding in Minnesota rivers. Sci Total Environ 368:138–148

    Article  CAS  PubMed  Google Scholar 

  • Bañuelos G, LeDuc DL, Pilon-Smits EAH, Terry N (2007) Transgenic Indian mustard overexpressing selenocysteine lyase or selenocysteine methyltransferase exhibit enhanced potential for selenium phytoremediation under field conditions. Environ Sci Technol 41:599–605

    Article  PubMed  CAS  Google Scholar 

  • Barceló J, Poschenrieder C (1990) Plant water relations as affected by heavy metal stress: a review. J Plant Nutr 13:1–37

    Article  Google Scholar 

  • Becher M, Talke IN, Krall L, Krämer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268

    Article  CAS  PubMed  Google Scholar 

  • Beneš I, Schreiber K, Ripperger H, Kircheiss A (1983) Metal complex formation by nicotianamine, a possible phytosiderophore. Experientia 39:261–262

    Article  Google Scholar 

  • Bentley R, Chasteen TG (2002) Microbial methylation of metalloids: arsenic, antimony, and bismuth. Microbiol Mol Biol Rev 66:250–271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernard C, Roosens N, Czernic P, Lebrun M, Verbruggen N (2004) A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Lett 569:140–148

    Article  CAS  PubMed  Google Scholar 

  • Bizily SP, Rugh CL, Summers AO, Meagher RB (1999) Phytoremediation of methylmercury pollution: merB expression in Arabidopsis thaliana confers resistance to organomercurials. Proc Natl Acad Sci U S A 96:6808–6813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bizily SP, Kim T, Kandasamy MK, Meagher RB (2003) Subcellular targeting of methylmercury lyase enhances its specific activity for organic mercury detoxification in plants. Plant Physiol 131:463–471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boening DW (2000) Ecological effects, transport, and fate of mercury: a general review. Chemosphere 40:1335–1351

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Booth S, Zeller D (2005) Mercury, food webs, and marine mammals: implications of diet and climate change for human health. Environ Health Perspect 113:521–526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bovet L, Eggmann T, Meylan-Bettex M, Polier J, Kammer P, Marin E, Feller U, Martinoia E (2003) Transcript levels of AtMRPs after cadmium treatment: induction of AtMRP3. Plant Cell Environ 26:371–381

    Article  CAS  Google Scholar 

  • Boxall ABA, Hardy A, Beulke S, Boucard T, Burgin L, Falloon PD, Haygarth PM, Hutchinson T, Kovats RS, Leonardi G et al (2009) Impacts of climate change on indirect human exposure to pathogens and chemicals from agriculture. Environ Health Perspect 117:508–514

    Article  CAS  PubMed  Google Scholar 

  • Boyer PD (1954) Spectrophotometric study of the reaction of protein sulfhydryl groups with organic mercurials. J Am Chem Soc 76:4331–4337

    Article  CAS  Google Scholar 

  • Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Buchanan B, Gruissem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 1158–1203

    Google Scholar 

  • Broeks A, Gerrard B, Allikmets R, Dean M, Plasterk RH (1996) Homologues of the human multidrug resistance genes MRP and MDR contribute to heavy metal resistance in the soil nematode Caenorhabditis elegans. EMBO J 15:6132–6143

    CAS  PubMed  PubMed Central  Google Scholar 

  • Callahan DL, Baker AJM, Kolev SD, Wedd AG (2006) Metal ion ligands in hyperaccumulating plants. J Biol Inorg Chem 11:2–12

    Article  CAS  PubMed  Google Scholar 

  • Casteel MJ, Sobsey MD, Mueller JP (2006) Fecal contamination of agricultural soils before and after hurricane-associated flooding in North Carolina. J Environ Sci Health A Tox Hazard Subst Environ Eng 41:173–184

    Article  CAS  PubMed  Google Scholar 

  • Catarecha P, Segura MD, Franco-Zorrilla JM, García-Ponce B, Lanza M, Solano R, Paz-Ares J, Leyva A (2007) A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. Plant Cell 19:1123–1133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chardonnens A, Koevoets P, van Zanten A, Schat H, Verkleij J (1999) Properties of enhanced tonoplast zinc transport in naturally selected zinc-tolerant Silene vulgaris. Plant Physiol 120:779–786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chatterjee J (2000) Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ Pollut 109:69–74

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Zhu YG, Liu WJ, Meharg AA (2005) Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (Oryza sativa) roots. New Phytol 165:91–97

    Article  CAS  PubMed  Google Scholar 

  • Choi J, Pak C, Lee CW (1996) Micro nutrient toxicity in French marigold. J Plant Nutr 19:901–916

    Article  CAS  Google Scholar 

  • Chu HH (2010) Analyses of Arabidopsis Yellow Stripe-Like (YSL) family of metal transporters. PhD dissertation (Amherst, MA: University of Massachusetts). Paper 159

    Google Scholar 

  • Clark GT, Dunlop J, Phung HT (2000) Phosphate absorption by Arabidopsis thaliana: interactions between phosphorus status and inhibition by arsenate. Funct Plant Biol 27:959–965

    Article  CAS  Google Scholar 

  • Clemens S, Kim EJ, Neumann D, Schroeder JI (1999) Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J 18:3325–3333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  CAS  PubMed  Google Scholar 

  • Cobbett CS, Meagher RB (2002) Arabidopsis and the genetic potential for the phytoremediation of toxic elemental and organic pollutants. Arabidopsis Book 1:e0032

    Article  PubMed  PubMed Central  Google Scholar 

  • Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346–349

    Article  CAS  PubMed  Google Scholar 

  • Das HK, Mitra AK, Sengupta PK, Hossain A, Islam F, Rabbani GH (2004) Arsenic concentrations in rice, vegetables, and fish in Bangladesh: a preliminary study. Environ Int 30:383–387

    Article  CAS  PubMed  Google Scholar 

  • De Vries W, Lofts S, Tipping E, Meili M, Groenenberg J, Schütze G (2007) Impact of soil properties on critical concentrations of cadmium, lead, copper, zinc, and mercury in soil and soil solution in view of ecotoxicological effects. Rev Environ Contam Toxicol SE-3. Springer, New York, pp 47–89

    Google Scholar 

  • Deinlein U, Weber M, Schmidt H, Rensch S, Trampczynska A, Hansen TH, Husted S, Schjoerring JK, Talke IN, Krämer U et al (2012) Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. Plant Cell 24:708–723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delhaize E (2003) Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. Plant Cell Online 15:1131–1142

    Article  CAS  Google Scholar 

  • Déportes I, Benoit-Guyod JL, Zmirou D (1995) Hazard to man and the environment posed by the use of urban waste compost: a review. Sci Total Environ 172:197–222

    Article  PubMed  Google Scholar 

  • Dhankher OP, Li Y, Rosen BP, Shi J, Salt D, Senecoff JF, Sashti NA, Meagher RB (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and gamma-glutamylcysteine synthetase expression. Nat Biotechnol 20:1140–1145

    Article  CAS  PubMed  Google Scholar 

  • Dhankher OP, Rosen BP, McKinney EC, Meagher RB (2006) Hyperaccumulation of arsenic in the shoots of Arabidopsis silenced for arsenate reductase (ACR2). Proc Natl Acad Sci U S A 103:5413–5418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dietz KJ, Baier M, Krämer U (1999) Free radicals and reactive oxygen species as mediators of heavy metal toxicity. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants: from molecules to ecosystems. Springer, Heidelberg, pp 73–97

    Chapter  Google Scholar 

  • Dixit AR, Dhankher OP (2011) A novel stress-associated protein “AtSAP10” from Arabidopsis thaliana confers tolerance to nickel, manganese, zinc, and high temperature stress. PLoS One 6:e20921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixit V, Pandey V, Shyam R (2002) Chromium ions inactivate electron transport and enhance superoxide generation in vivo in pea (Pisum sativum L. cv. Azad) root mitochondria. Plant Cell Environ 25:687–693

    Article  CAS  Google Scholar 

  • Dong J, Wu F, Zhang G (2006) Influence of cadmium on antioxidant capacity and four microelement concentrations in tomato seedlings (Lycopersicon esculentum). Chemosphere 64:1659–1666

    Article  CAS  PubMed  Google Scholar 

  • Dräger DB, Desbrosses-Fonrouge AG, Krach C, Chardonnens AN, Meyer RC, Saumitou-Laprade P, Krämer U (2004) Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J 39:425–439

    Article  PubMed  CAS  Google Scholar 

  • Ebbs SD, Kochian LV (1997) Toxicity of zinc and copper to Brassica species: implications for phytoremediation. J Environ Qual 26:776

    Article  CAS  Google Scholar 

  • Ellis DR, Salt DE (2003) Plants, selenium and human health. Curr Opin Plant Biol 6:273–279

    Article  CAS  PubMed  Google Scholar 

  • Eren E, Argüello JM (2004) Arabidopsis HMA2, a divalent heavy metal-transporting P(IB)-type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol 136:3712–3723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evanko CR, Dzombak DA (1997) Remediation of metals- contaminated soils and groundwater. Technology Evaluation Report(TE-97-01). Ground-Water Remediation Technologies Analysis Center (GWRTAC), Pittsburgh

    Google Scholar 

  • Falchuk KH, Goldwater LJ, Vallee BL (1977) The biochemistry and toxicology of mercury. In: McAuliffe CA (ed) The biochemical and toxicology mercury. Macmillan, New York, pp 261–284

    Google Scholar 

  • Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, Dietz KJ (2005) The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J Biol Chem 280:12168–12180

    Article  CAS  PubMed  Google Scholar 

  • Fomina M, Hillier S, Charnock JM, Melville K, Alexander IJ, Gadd GM (2005) Role of oxalic acid overexcretion in transformations of toxic metal minerals by Beauveria caledonica. Appl Environ Microbiol 71:371–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fontes RLF, Cox FR (1998) Zinc toxicity in soybean grown at high iron concentration in nutrient solution. J Plant Nutr 21:1723–1730

    Article  CAS  Google Scholar 

  • Fordyce FM (2005) Selenium deficiency and toxicity in the environment. In: Selinus O (ed) Essentials of medical geology. Elsevier, Amsterdam, pp 373–415

    Google Scholar 

  • Freeman JL, Persans MW, 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 16:2176–2191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freeman JL, Garcia D, Kim D, Hopf A, Salt DE (2005) Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiol 137:1082–1091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh M, Shen J, Rosen BP (1999) Pathways of As(III) detoxification in Saccharomyces cerevisiae. Proc Natl Acad Sci 96:5001–5006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gill SS, Tuteja N (2011) Cadmium stress tolerance in crop plants probing the role of sulfur. Plant Signal Behav 6:215–222

    Article  CAS  PubMed  Google Scholar 

  • Gisbert C, Ros R, De Haro A, Walker DJ, Pilar Bernal M, Serrano R, Navarro-Aviñó J (2003) A plant genetically modified that accumulates Pb is especially promising for phytoremediation. Biochem Biophys Res Commun 303:440–445

    Article  CAS  PubMed  Google Scholar 

  • Greger M, Ogren E (1991) Direct and indirect effects of Cd2+ on photosynthesis in sugar beet (Beta vulgaris). Physiol Plant 83:129–135

    Article  CAS  Google Scholar 

  • Grennan AK (2011) Metallothioneins, a diverse protein family. Plant Physiol 155:1750–1751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grill E, Winnacker EL, Zenk MH (1985) Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science 230:674–676

    Article  CAS  PubMed  Google Scholar 

  • Grill E, Loffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Natl Acad Sci 86:6838–6842

    Google Scholar 

  • Grispen VMJ, Irtelli B, Hakvoort HWJ, Vooijs R, Bliek T, ten Bookum WM, Verkleij JAC, Schat H (2009) Expression of the Arabidopsis metallothionein 2b enhances arsenite sensitivity and root to shoot translocation in tobacco. Environ Exp Bot 66:69–73

    Article  CAS  Google Scholar 

  • Grotz N, Fox T, Connolly E, Park W, Guerinot ML, Eide D (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc Natl Acad Sci 95:7220–7224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu JG, Zhao X, Wang X (2003) Reused path of heavy metal pollution in soils and its research advance. J Basic Sci Eng 11:143–151

    Google Scholar 

  • Gueldry O, Lazard M, Delort F, Dauplais M, Grigoras I, Blanquet S, Plateau P (2003) Ycf1p-dependent Hg(II) detoxification in Saccharomyces cerevisiae. Eur J Biochem 270:2486–2496

    Article  CAS  PubMed  Google Scholar 

  • Guerinot ML, Salt DE (2001) Fortified foods and phytoremediation. Two sides of the same coin. Plant Physiol 125:164–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo J, Dai X, Xu W, Ma M (2008) Overexpressing GSH1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere 72:1020–1026

    Article  CAS  PubMed  Google Scholar 

  • Guo J, Xu W, Ma M (2012) The assembly of metals chelation by thiols and vacuolar compartmentalization conferred increased tolerance to and accumulation of cadmium and arsenic in transgenic Arabidopsis thaliana. J Hazard Mater 199–200:309–313

    Article  PubMed  CAS  Google Scholar 

  • Guo J, Xu L, Su Y, Wang H, Gao S, Xu J, Que Y (2013) ScMT2-1-3, a metallothionein gene of sugarcane, plays an important role in the regulation of heavy metal tolerance/accumulation. Biomed Res Int. doi:10.1155/2013/904769

    Google Scholar 

  • Gupta DK, Huang HG, Yang XE, Razafindrabe BHN, Inouhe M (2010) The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione. J Hazard Mater 177:437–444

    Article  CAS  PubMed  Google Scholar 

  • Ha SB (1999) Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell Online 11:1153–1164

    Article  CAS  Google Scholar 

  • Haag-Kerwer A, Schafer HJ, Heiss S, Walter C, Rausch T (1999) Cadmium exposure in Brassica juncea causes a decline in transpiration rate and leaf expansion without effect on photosynthesis. J Exp Bot 50:1827–1835

    Article  CAS  Google Scholar 

  • Hale KL, McGrath SP, Lombi E, Stack SM, Terry N, Pickering IJ, George GN, Pilon-Smits EA (2001) Molybdenum sequestration in Brassica species. A role for anthocyanins? Plant Physiol 126:1391–1402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall JLL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  CAS  PubMed  Google Scholar 

  • Hammerschmidt CR, Fitzgerald WF, Lamborg CH, Balcom PH, Tseng CM (2006) Biogeochemical cycling of methylmercury in lakes and tundra watersheds of Arctic Alaska. Environ Sci Technol 40:1204–1211

    Article  CAS  PubMed  Google Scholar 

  • Hanikenne M, Motte P, Wu MCS, Wang T, Loppes R, Matagne RF (2005) A mitochondrial half-size ABC transporter is involved in cadmium tolerance in Chlamydomonas reinhardtii. Plant Cell Environ 28:863–873

    Article  CAS  Google Scholar 

  • Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266

    Article  PubMed  CAS  Google Scholar 

  • Harmon SM, Wyatt DE (2008) Evaluation of post-Katrina flooded soils for contaminants and toxicity to the soil invertebrates Eisenia fetida and Caenorhabditis elegans. Chemosphere 70:1857–1864

    Article  CAS  PubMed  Google Scholar 

  • Hart BA, Lee CH, Shukla GS, Shukla A, Osier M, Eneman JD, Chiu JF (1999) Characterization of cadmium-induced apoptosis in rat lung epithelial cells: evidence for the participation of oxidant stress. Toxicology 133:43–58

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa I, Terada E, Sunairi M, Wakita H, Shinmachi F, Noguchi A, Nakajima M, Yazaki J (1997) Genetic improvement of heavy metal tolerance in plants by transfer of the yeast metallothionein gene (CUP1). In: Ando T, Fujita K, Mae T, Matsumoto H, Mori S, Sekiya J (eds) Plant nutrition for sustainable food production and environment SE – 117. Springer, Dordrecht, pp 391–395

    Chapter  Google Scholar 

  • Hawkesford MJ (2003) Transporter gene families in plants: the sulphate transporter gene family – redundancy or specialization? Physiol Plant 117:155–163

    Article  CAS  Google Scholar 

  • Haydon MJ, Cobbett CS (2007a) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506

    Article  CAS  PubMed  Google Scholar 

  • Haydon MJ, Cobbett CS (2007b) A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis. Plant Physiol 143:1705–1719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heaton ACP, Rugh CL, Kim T, Wang NJ, Meagher RB (2003) Toward detoxifying mercury-polluted aquatic sediments with rice genetically engineered for mercury resistance. Environ Toxicol Chem 22:2940–2947

    Article  CAS  PubMed  Google Scholar 

  • Heckathorn SA, Mueller JK, Laguidice S, Zhu B, Barrett T, Blair B, Dong Y (2004) Chloroplast small heat-shock proteins protect photosynthesis during heavy metal stress. Am J Bot 91:1312–1318

    Article  CAS  PubMed  Google Scholar 

  • Hegedüs A, Erdei S, Horváth G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci 160:1085–1093

    Article  PubMed  Google Scholar 

  • Hilscherova K, Dusek L, Kubik V, Cupr P, Hofman J, Klanova J, Holoubek I (2007) Redistribution of organic pollutants in river sediments and alluvial soils related to major floods. J Soils Sediments 7:167–177

    Article  CAS  Google Scholar 

  • Howden R (1995) Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol 107:1059–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang TL, Huang HJ (2008) ROS and CDPK-like kinase-mediated activation of MAP kinase in rice roots exposed to lead. Chemosphere 71:1377–1385

    Article  CAS  PubMed  Google Scholar 

  • Huang B, Hatch E, Goldsbrough PB (1987) Selection and characterization of cadmium tolerant cells in tomato. Plant Sci 52:211–221

    Article  CAS  Google Scholar 

  • Huang J, Zhang Y, Peng J-S, Zhong C, Yi H-Y, Ow DW, Gong J-M (2012) Fission yeast HMT1 lowers seed cadmium through phytochelatin-dependent vacuolar sequestration in Arabidopsis. Plant Physiol 158:1779–1788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, Young J, Camakaris J, Harper JF, Cobbett CS (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Indriolo E, Na G, Ellis D, Salt DE, Banks JA (2010) A vacuolar arsenite transporter necessary for arsenic tolerance in the arsenic hyperaccumulating fern Pteris vittata is missing in flowering plants. Plant Cell 22:2045–2057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishimaru Y, Suzuki M, Kobayashi T, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2005) OsZIP4, a novel zinc-regulated zinc transporter in rice. J Exp Bot 56:3207–3214

    Article  CAS  PubMed  Google Scholar 

  • Kaiser J (2001) Environmental health. Second look at arsenic finds higher risk. Science 293:2189

    Article  CAS  PubMed  Google Scholar 

  • Kampfenkel K, Van Montagu M, Inze D (1995) Effects of iron excess on Nicotiana plumbaginifolia plants (implications to oxidative stress). Plant Physiol 107:725–735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanneganti V, Gupta AK (2008) Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice. Plant Mol Biol 66:445–462

    Article  CAS  PubMed  Google Scholar 

  • Kathuria H, Giri J, Tyagi H, Tyagi AK (2007) Advances in transgenic rice biotechnology. CRC Crit Rev Plant Sci 26:65–103

    Article  CAS  Google Scholar 

  • Keating M, Mahaffey K, Schoeny R, Rice GE, Bullock OR (1997) Mercury study report to congress, vol 1. Executive summary, EPA-452/R-97-003, United States Environmental Protection Agency, Research Triangle Park, NC

    Google Scholar 

  • 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 39:237–251

    Article  CAS  PubMed  Google Scholar 

  • Kim DY, Bovet L, Kushnir S, Noh EW, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140:922–932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim DY, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 50:207–218

    Article  CAS  PubMed  Google Scholar 

  • Kneer R, Zenk MH (1992) Phytochelatins protect plant enzymes from heavy metal poisoning. Phytochemistry 31:2663–2667

    Article  CAS  Google Scholar 

  • Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol Biol 40:37–44

    Article  CAS  PubMed  Google Scholar 

  • Kotrba P, Najmanova J, Macek T, Ruml T, Mackova M (2009) Genetically modified plants in phytoremediation of heavy metal and metalloid soil and sediment pollution. Biotechnol Adv 27:799–810

    Article  CAS  PubMed  Google Scholar 

  • Krämer U, Clemens S (2006) Functions and homeostasis of zinc, copper, and nickel in plants. In: Tamas M, Martinoia E (eds) Molecular biology of metal homeostasis and detoxification SE-96. Springer, Berlin/Heidelberg, pp 216–271

    Google Scholar 

  • Kramer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith JAC (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638

    Article  CAS  Google Scholar 

  • 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. Plant Physiol 115:1641–1650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krämer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272

    Article  PubMed  CAS  Google Scholar 

  • Krupa Z (1988) Cadmium-induced changes in the composition and structure of the light-harvesting chlorophyll a/b protein complex II in radish cotyledons. Physiol Plant 73:518–524

    Article  CAS  Google Scholar 

  • Krupa Z, Oquist G, Huner NPA (1993) The effects of cadmium on photosynthesis of Phaseolus vulgaris – a fluorescence analysis. Physiol Plant 88:626–630

    Article  CAS  Google Scholar 

  • Küpper H, Mijovilovich A, Meyer-Klaucke W, Kroneck PMH (2004) Tissue- and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by x-ray absorption spectroscopy. Plant Physiol 134:748–757

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuroda T, Tsuchiya T (2009) Multidrug efflux transporters in the MATE family. Biochim Biophys Acta 1794:763–768

    Article  CAS  PubMed  Google Scholar 

  • Larsen E, Moseholm L, Nielsen M (1992) Atmospheric deposition of trace elements around point sources and human health risk assessment. II: uptake of arsenic and chromium by vegetables grown near a wood preservation factory. Sci Total Environ 126:263–275

    Article  CAS  PubMed  Google Scholar 

  • LeBlanc MS, McKinney EC, Meagher RB, Smith AP (2013) Hijacking membrane transporters for arsenic phytoextraction. J Biotechnol 163:1–9

    Article  CAS  PubMed  Google Scholar 

  • LeDuc DL, Tarun AS, Montes-Bayon M, Meija J, Malit MF, Wu CP, AbdelSamie M, Chiang CY, Tagmount A, deSouza M et al (2004) Overexpression of selenocysteine methyltransferase in Arabidopsis and Indian mustard increases selenium tolerance and accumulation. Plant Physiol 135:377–383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LeDuc DL, AbdelSamie M, Montes-Bayon M, Wu CP, Reisinger SJ, Terry N (2006) Overexpressing both ATP sulfurylase and selenocysteine methyltransferase enhances selenium phytoremediation traits in Indian mustard. Environ Pollut 144:70–76

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Kang BS (2005) Phytochelatin is not a primary factor in determining copper tolerance. J Plant Biol 48:32–38

    Article  CAS  Google Scholar 

  • Lee CW, Choi JM, Pak CH (1996) Micronutrient toxicity in seed geranium (Pelargonium x hortorum Bailey). J Am Soc Hort Sci 121:77–82

    CAS  Google Scholar 

  • Lee S, Moon JS, Ko TS, Petros D, Goldsbrough PB, Korban SS (2003) Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiol 131:656–663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J, Shim D, Song WY, Hwang I, Lee Y (2004) Arabidopsis metallothioneins 2a and 3 enhance resistance to cadmium when expressed in Vicia faba guard cells. Plant Mol Biol 54:805–815

    Article  CAS  PubMed  Google Scholar 

  • Lee M, Lee K, Lee J, Noh EW, Lee Y (2005) AtPDR12 contributes to lead resistance in Arabidopsis. Plant Physiol 138:827–836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lefebvre DD, Laliberte JF (1987) Mammalian metallothionein functions in plants. In: Verma D, Brisson N (eds) Molecular genetic of plant-microbe interactions SE-7. Springer, Dordrecht, pp 32–34

    Chapter  Google Scholar 

  • Leitenmaier B, Küpper H (2013) Compartmentation and complexation of metals in hyperaccumulator plants. Front Plant Sci 4:1–13

    Article  Google Scholar 

  • Li ZS, Szczypka M, Lu YP, Thiele DJ, Rea PA (1996) The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S-conjugate pump. J Biol Chem 271:6509–6517

    Article  CAS  PubMed  Google Scholar 

  • Li ZS, Lu YP, Zhen RG, Szczypka M, Thiele DJ, Rea PA (1997) A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis (glutathionato) cadmium. Proc Natl Acad Sci U S A 94:42–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Dhankher OP, Carreira L, Balish RS, Meagher RB (2005) Arsenic and mercury tolerance and cadmium sensitivity in Arabidopsis plants expressing bacterial gamma-glutamylcysteine synthetase. Environ Toxicol Chem 24:1376

    Article  CAS  PubMed  Google Scholar 

  • Li T, Xu Z, Han X, Yang X, Sparks DL (2012) Characterization of dissolved organic matter in the rhizosphere of hyperaccumulator Sedum alfredii and its effect on the mobility of zinc. Chemosphere 88:570–576

    Article  CAS  PubMed  Google Scholar 

  • Liao MT, Hedley MJ, Woolley DJ, Brooks RR, Nichols MA (2000) Copper uptake and translocation in chicory (Cichorium intybus L. cv Grasslands Puna) and tomato (Lycopersicon esculentum Mill. cv Rondy) plants grown in NFT system. II. The role of nicotianamine and histidine in xylem sap copper transport. Plant Soil 223:245–254

    Article  Google Scholar 

  • Lin R, Wang X, Luo Y, Du W, Guo H, Yin D (2007) Effects of soil cadmium on growth, oxidative stress and antioxidant system in wheat seedlings (Triticum aestivum L.). Chemosphere 69:89–98

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Cotgreave I, Atzori L, Grafström RC (1992) The mechanism of Hg2+ toxicity in cultured human oral fibroblasts: the involvement of cellular thiols. Chem Biol Interact 85:69–78

    Article  CAS  PubMed  Google Scholar 

  • Magalhaes JV, Liu J, Guimaraes CT, Lana UG, Alves VM, Wang YH, Kochian LV (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39:1156–1161

    Article  CAS  PubMed  Google Scholar 

  • Manara A (2012) Plant responses to heavy metal toxicity. In: Furini A (ed) Plants and heavy metals, Briefs in molecular science. Springer, Dordrecht, pp 27–53

    Chapter  Google Scholar 

  • Marin AR, Pezeshki SR, Masschelen PH, Choi HS (1993) Effect of dimethylarsenic acid (DMAA) on growth, tissue arsenic, and photosynthesis of rice plants. J Plant Nutr 16:865–880

    Article  CAS  Google Scholar 

  • Martínez M, Bernal P, Almela C, Vélez D, García-Agustín P, Serrano R, Navarro-Aviñó J (2006) An engineered plant that accumulates higher levels of heavy metals than Thlaspi caerulescens, with yields of 100 times more biomass in mine soils. Chemosphere 64:478–485

    Article  PubMed  CAS  Google Scholar 

  • Maser P (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meharg AA, Macnair MR (1992) Suppression of the high affinity phosphate uptake system: a mechanism of arsenate tolerance in Holcus lanatus L. J Exp Bot 43:519–524

    Article  CAS  Google Scholar 

  • Mendoza-Cózatl DG, Xie Q, Akmakjian GZ, Jobe TO, Patel A, Stacey MG, Song L, Demoin DW, Jurisson SS, Stacey G et al (2014) OPT3 is a component of the iron-signaling network between leaves and roots and misregulation of OPT3 leads to an over-accumulation of cadmium in seeds. Mol Plant 7:1455–1469

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mijovilovich A, Leitenmaier B, Meyer-Klaucke W, Kroneck PMH, Götz B, Küpper H (2009) Complexation and toxicity of copper in higher plants. II. Different mechanisms for copper versus cadmium detoxification in the copper-sensitive cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges Ecotype). Plant Physiol 151:715–731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller AF (2012) Superoxide dismutases: ancient enzymes and new insights. FEBS Lett 586:585–595

    Article  CAS  PubMed  Google Scholar 

  • Mills RF, Francini A, Ferreira da Rocha PSC, Baccarini PJ, Aylett M, Krijger GC, Williams LE (2005) The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett 579:783–791

    Article  CAS  PubMed  Google Scholar 

  • Minamata Disease Research Group (1968) Minamata Disease Research Group: Minamata Disease. Medical School of Kumamoto University, Kumamoto

    Google Scholar 

  • Minglin L, Yuxiu Z, Tuanyao C (2005) Identification of genes up-regulated in response to Cd exposure in Brassica juncea L. Gene 363:151–158

    Article  PubMed  CAS  Google Scholar 

  • Misra S, Gedamu L (1989) Heavy metal tolerant transgenic Brassica napus L. and Nicotiana tabacum L. plants. Theor Appl Genet 78:161–168

    Article  CAS  PubMed  Google Scholar 

  • Mizuno T, Usui K, Horie K, Nosaka S, Mizuno N, Obata H (2005) Cloning of three ZIP/Nramp transporter genes from a Ni hyperaccumulator plant Thlaspi japonicum and their Ni2+-transport abilities. Plant Physiol Biochem 43:793–801

    Article  CAS  PubMed  Google Scholar 

  • Morel M, Crouzet J, Gravot A, Auroy P, Leonhardt N, Vavasseur A, Richaud P (2009) AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol 149:894–904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci U S A 101:6309–6314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ng BH, Anderson JW (1979) Light-dependent incorporation of selenite and sulphite into selenocysteine and cysteine by isolated pea chloroplasts. Phytochemistry 18:573–580

    Article  CAS  Google Scholar 

  • Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339

    Article  CAS  PubMed  Google Scholar 

  • Ortiz DF, Kreppel L, Speiser DM, Scheel G, McDonald G, Ow DW (1992) Heavy metal tolerance in the fission yeast requires an ATP-binding cassette-type vacuolar membrane transporter. Embo J 11:3491–3499

    CAS  PubMed  PubMed Central  Google Scholar 

  • Papadopoulou B, Roy G, Dey S, Rosen B, Ouellette M (1994) Contribution of the Leishmania P-glycoprotein-related gene ltpgpA to oxyanion resistance. J Biol Chem 269:11980–11986

    CAS  PubMed  Google Scholar 

  • 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 136:3814–3823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park J, Song W-Y, Ko D, Eom Y, Hansen TH, Schiller M, Lee TG, Martinoia E, Lee Y (2012) The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J 69:278–288

    Article  CAS  PubMed  Google Scholar 

  • Patra M, Sharma A (2000) Mercury toxicity in plants. Bot Rev 66:379–422

    Article  Google Scholar 

  • Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ Exp Bot 52:199–223

    Article  CAS  Google Scholar 

  • Paulose B, Jaiwal PK, Dhankher OP (2008) Heavy metal transporters in plants. In: Jaiwal S, Dhankher OP (eds) Plant membrane and vacuolar transporters. CABI, Wallingford/Cambridge, pp 213–238

    Chapter  Google Scholar 

  • Paulose B, Chhikara S, Coomey J, Jung HI, Vatamaniuk O, Dhankher OP (2013) A γ-glutamyl cyclotransferase protects Arabidopsis plants from heavy metal toxicity by recycling glutamate to maintain glutathione homeostasis. Plant Cell 25:4580–4595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peer WA, Mamoudian M, Lahner B, Reeves RD, Murphy AS, Salt DE (2003) Identifying model metal hyperaccumulating plants: germplasm analysis of 20 Brassicaceae accessions from a wide geographical area. New Phytol 159:421–430

    Article  CAS  Google Scholar 

  • Pich A, Scholz G, Stephan UW (1994) Iron-dependent changes of heavy metals, nicotianamine, and citrate in different plant organs and in the xylem exudate of two tomato genotypes. Nicotianamine as possible copper translocator. Plant Soil 165:189–196

    Article  CAS  Google Scholar 

  • Pilon-Smits EAHE, Hwang S, Mel Lytle C, Zhu Y, Tai J, Bravo R, Chen Y, Leustek T, Terry N (1999) Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol 119:123–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pineau C, Loubet S, Lefoulon C, Chalies C, Fizames C, Lacombe B, Ferrand M, Loudet O, Berthomieu P, Richard O (2012) Natural variation at the FRD3 MATE transporter locus reveals cross-talk between Fe homeostasis and Zn tolerance in Arabidopsis thaliana. PLoS Genet 8:e1003120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pomponi M, Censi V, Di Girolamo V, De Paolis A, di Toppi LS, Aromolo R, Costantino P, Cardarelli M (2006) Overexpression of Arabidopsis phytochelatin synthase in tobacco plants enhances Cd2+ tolerance and accumulation but not translocation to the shoot. Planta 223:180–190

    Article  CAS  PubMed  Google Scholar 

  • Prasad MNV (1995) Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 35:525–545

    Article  CAS  Google Scholar 

  • Rauser WE (1995) Phytochelatins and related peptides: structure, biosynthesis, and function. Plant Physiol 109:1141–1149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rauser WE (1999) Structure and function of metal chelators produced by plants: the case for organic acids, amino acids, phytin, and metallothioneins. Cell Biochem Biophys 31:19–48

    Article  CAS  PubMed  Google Scholar 

  • Robinson NJ, Tommey AM, Kuske C, Jackson PJ (1993) Plant metallothioneins. Biochem J 295(Pt 1):1–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Pazmiño DM, Testillano PS, Risueño MC, Del Río LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229–243

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci U S A 97:12356–12360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rose JB, Epstein PR, Lipp EK, Sherman BH, Bernard SM, Patz JA (2001) Climate variability and change in the United States: potential impacts on water- and foodborne diseases caused by microbiologic agents. Environ Health Perspect 109(Suppl):211–221

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosen BP (1999) Families of arsenic transporters. Trends Microbiol 7:207–212

    Article  CAS  PubMed  Google Scholar 

  • Rugh CL (2001) Mercury detoxification with transgenic plants and other biotechnological breakthroughs for phytoremediation. Vitro Cell Dev Biol Plant 37:321–325

    Article  CAS  Google Scholar 

  • Rugh CL, Wilde HD, Stack NM, Thompson DM, Summers AO, Meagher RB (1996) Mercuric ion reduction and resistance in transgenic Arabidopsis thaliana plants expressing a modified bacterial merA gene. Proc Natl Acad Sci U S A 93:3182–3187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz ON, Hussein HS, Terry N, Daniell H (2003) Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Physiol 132:1344–1352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryan PR, Raman H, Gupta S, Horst WJ, Delhaize E (2009) A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol 149:340–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salt DE, Thurman DA, Tomsett AB, Sewell AK (1989) Copper phytochelatins of Mimulus guttatus. Proc R Soc B Biol Sci 236:79–89

    Article  CAS  Google Scholar 

  • Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salt DE, Prince RC, Baker AJM, Raskin I, Pickering IJ (1999) Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using x-ray absorption spectroscopy. Environ Sci Technol 33:713–717

    Article  CAS  Google Scholar 

  • Schaaf G, Ludewig U, Erenoglu BE, Mori S, Kitahara T, von Wirén N (2004) ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J Biol Chem 279:9091–9096

    Article  CAS  PubMed  Google Scholar 

  • Schat H (2002) The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. J Exp Bot 53:2381–2392

    Article  CAS  PubMed  Google Scholar 

  • Schmoger MEV (2000) Detoxification of arsenic by phytochelatins in plants. Plant Physiol 122:793–802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    PubMed  Google Scholar 

  • Schwartz MS, Benci JL, Selote DS, Sharma AK, Chen AGY, Dang H, Fares H, Vatamaniuk OK (2010) Detoxification of multiple heavy metals by a half-molecule ABC transporter, HMT-1, and coelomocytes of Caenorhabditis elegans. PLoS One 5:e9564

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Scoccianti V, Crinelli R, Tirillini B, Mancinelli V, Speranza A (2006) Uptake and toxicity of Cr(III) in celery seedlings. Chemosphere 64:1695–1703

    Article  CAS  PubMed  Google Scholar 

  • Sekhar K, Priyanka B, Reddy VD, Rao KV (2011) Metallothionein 1 (CcMT1) of pigeonpea (Cajanus cajan L.) confers enhanced tolerance to copper and cadmium in Escherichia coli and Arabidopsis thaliana. Environ Exp Bot 72:131–139

    Article  CAS  Google Scholar 

  • Setya A, Murillo M, Leustek T (1996) Sulfate reduction in higher plants: molecular evidence for a novel 5′-adenylylsulfate reductase. Proc Natl Acad Sci 93:13383–13388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753

    Article  CAS  PubMed  Google Scholar 

  • Sharma D, Sharma C, Tripathi R (2003) Phytotoxic lesions of chromium in maize. Chemosphere 51:63–68

    Article  CAS  PubMed  Google Scholar 

  • Shim D, Hwang JU, Lee J, Lee S, Choi Y, An G, Martinoia E, Lee Y (2009) Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell 21:4031–4043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 39:629–642

    Article  CAS  PubMed  Google Scholar 

  • Shu X, Yin L, Zhang Q, Wang W (2012) Effect of Pb toxicity on leaf growth, antioxidant enzyme activities, and photosynthesis in cuttings and seedlings of Jatropha curcas L. Environ Sci Pollut Res Int 19:893–902

    Article  CAS  PubMed  Google Scholar 

  • Singh S, Verma A, Dubey VK (2012) Effectivity of anti-oxidative enzymatic system on diminishing the oxidative stress induced by aluminium in chickpea (Cicer arietinum L.) seedlings. Braz J Plant Physiol 24:47–54

    Article  CAS  Google Scholar 

  • Smith FW, Ealing PM, Hawkesford MJ, Clarkson DT (1995) Plant members of a family of sulfate transporters reveals functional subtypes. Proc Natl Acad Sci U S A 92:9373–9377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song WY, Sohn EJ, Martinoia E, Lee YJ, Yang YY, Jasinski M, Forestier C, Hwang I, Lee Y (2003) Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nat Biotechnol 21:914–919

    Article  CAS  PubMed  Google Scholar 

  • Song WY, 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 135:1027–1039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song WY, Park J, Mendoza-Cózatl DG, Suter-Grotemeyer M, Shim D, Hörtensteiner S, Geisler M, Weder B, Rea PA, Rentsch D et al (2010) Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc Natl Acad Sci U S A 107:21187–21192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stacey MG, Patel A, McClain WE, Mathieu M, Remley M, Rogers EE, Gassmann W, Blevins DG, Stacey G (2008) The Arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiol 146:589–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stadtman ER, Oliver CN (1991) Metal-catalyzed oxidation of proteins. Physiological consequences. J Biol Chem 266:2005–2008

    CAS  PubMed  Google Scholar 

  • Steffens JC (1990) The heavy metal-binding peptides of plants. Annu Rev Plant Physiol Plant Mol Biol 41:553–575

    Article  CAS  Google Scholar 

  • Summers AO (1986) Organization, expression, and evolution of genes for mercury resistance. Annu Rev Microbiol 40:607–634

    Article  CAS  PubMed  Google Scholar 

  • Szczypka M, Wemmie J, Moye-Rowley W, Thiele D (1994) A yeast metal resistance protein similar to human cystic fibrosis transmembrane conductance regulator (CFTR) and multidrug resistance-associated protein. J Biol Chem 269:22853–22857

    CAS  PubMed  Google Scholar 

  • Terry N, Zayed AM, De Souza MP, Tarun AS (2000) Selenium in higher plants. Annu Rev Plant Physiol Plant Mol Biol 51:401–432

    Article  CAS  PubMed  Google Scholar 

  • Thomas JC, Davies EC, Malick FK, Endreszl C, Williams CR, Abbas M, Petrella S, Swisher K, Perron M, Edwards R et al (2003) Yeast metallothionein in transgenic tobacco promotes copper uptake from contaminated soils. Biotechnol Prog 19:273–280

    Article  CAS  PubMed  Google Scholar 

  • Thomine S, Lelièvre F, Debarbieux E, Schroeder JI, Barbier-Brygoo H (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34:685–695

    Article  CAS  PubMed  Google Scholar 

  • Tommasini R, Vogt E, Fromenteau M, Hörtensteiner S, Matile P, Amrhein N, Martinoia E (1998) An ABC-transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. Plant J 13:773–780

    Article  CAS  PubMed  Google Scholar 

  • Tommey AM, Shi J, Lindsay WP, Urwin PE, Robinson NJ (1991) Expression of the pea gene PSMTA in E. coli. Metal-binding properties of the expressed protein. FEBS Lett 292:48–52

    Article  CAS  PubMed  Google Scholar 

  • Trampczynska A, Küpper H, Meyer-Klaucke W, Schmidt H, Clemens S (2010) Nicotianamine forms complexes with Zn(II) in vivo. Metallomics 2:57–66

    Article  CAS  PubMed  Google Scholar 

  • Tseng TS, Tzeng SS, Yeh KW, Yeh CH, Chang FC, Chen YM, Lin CY (1993) The heat-shock response in rice seedlings: isolation and expression of cDNAs that encode Class I low-molecular-weight heat-shock proteins. Plant Cell Physiol 34:165–168

    CAS  Google Scholar 

  • Van Assche F, Clijsters H (1987) Enzyme analysis in plants as a tool for assessing phytotoxicity of heavy metal polluted soils. Med Fac Landbouww Rijksuniv Gent 52:1819–1824

    Google Scholar 

  • Van der Zaal BJ, Neuteboom LW, Pinas JE, Chardonnens AN, Schat H, Verkleij JA, Hooykaas PJ (1999) Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol 119:1047–1055

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Huysen T, Abdel-Ghany S, Hale KL, LeDuc D, Terry N, Pilon-Smits EAH (2003) Overexpression of cystathionine-gamma-synthase enhances selenium volatilization in Brassica juncea. Planta 218:71–78

    Article  PubMed  CAS  Google Scholar 

  • Van Nguyen N, Ferrero A (2006) Meeting the challenges of global rice production. Paddy Water Environ 4:1–9

    Article  Google Scholar 

  • Vatamaniuk OK, Mari S, Lu YP, Rea PA (1999) AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proc Natl Acad Sci U S A 96:7110–7115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 280:23684–23690

    Article  CAS  PubMed  Google Scholar 

  • Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richaud P (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312

    Article  CAS  PubMed  Google Scholar 

  • Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620

    Article  CAS  Google Scholar 

  • Vij S, Tyagi AK (2006) Genome-wide analysis of the stress associated protein (SAP) gene family containing A20/AN1 zinc-finger(s) in rice and their phylogenetic relationship with Arabidopsis. Mol Genet Genomics 276:565–575

    Article  CAS  PubMed  Google Scholar 

  • Vögeli-Lange R, Wagner GJ (1990) Subcellular localization of cadmium and cadmium-binding peptides in tobacco leaves: implication of a transport functions for cadmium-binding peptides. Plant Physiol 92:1086–1093

    Article  PubMed  PubMed Central  Google Scholar 

  • Von Wiren N (1999) Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants. Plant Physiol 119:1107–1114

    Article  Google Scholar 

  • Wang J, Zhao FJ, Meharg AA, Raab A, Feldmann J, McGrath SP (2002) Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol 130:1552–1561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wawrzynski A, Kopera E, Wawrzynska A, Kaminska J, Bal W, Sirko A (2006) Effects of simultaneous expression of heterologous genes involved in phytochelatin biosynthesis on thiol content and cadmium accumulation in tobacco plants. J Exp Bot 57:2173–2182

    Article  CAS  PubMed  Google Scholar 

  • Weber M, Harada E, Vess C, Roepenack-Lahaye EV, 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 37:269–281

    Article  CAS  PubMed  Google Scholar 

  • Wenzel W, Jockwer F (1999) Accumulation of heavy metals in plants grown on mineralised soils of the Austrian Alps. Environ Pollut 104:145–155

    Article  CAS  Google Scholar 

  • Wilber CG (1980) Toxicology of selenium: a review. Clin Toxicol 17:171–230

    Article  CAS  PubMed  Google Scholar 

  • Wilber C (1983) Selenium: a potential environmental poison and a necessary food constituent. Charles C Thomas Pub Ltd, Springfield

    Google Scholar 

  • Williams PN, Price AH, Raab A, Hossain SA, Feldmann J, Meharg AA (2005) Variation in arsenic speciation and concentration in paddy rice related to dietary exposure. Environ Sci Technol 39:5531–5540

    Article  CAS  PubMed  Google Scholar 

  • Wong CKE, Jarvis RS, Sherson SM, Cobbett CS (2009) Functional analysis of the heavy metal binding domains of the Zn/Cd-transporting ATPase, HMA2, in Arabidopsis thaliana. New Phytol 181:79–88

    Article  CAS  PubMed  Google Scholar 

  • Xiong XZ, Li PJ, Wang YS, Ten H, Wang LP, Song SH (1987) Environmental capacity of arsenic in soil and mathematical model. Huanjing Kexue 8:8–14

    CAS  Google Scholar 

  • Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South Afr J Bot 76:167–179

    Article  CAS  Google Scholar 

  • Yang Z, Wu Y, Li Y, Ling HQ, Chu C (2009) OsMT1a, a type 1 metallothionein, plays the pivotal role in zinc homeostasis and drought tolerance in rice. Plant Mol Biol 70:219–229

    Article  CAS  PubMed  Google Scholar 

  • Zayed AM, Terry N (1992) Selenium volatilization in broccoli as influenced by sulfate supply. J Plant Physiol 140:646–652

    Article  CAS  Google Scholar 

  • Zayed A, Lytle CM, Terry N (1998) Accumulation and volatilization of different chemical species of selenium by plants. Planta 206:284–292

    Article  CAS  Google Scholar 

  • Zhai Z, Gayomba SR, Jung HI, Vimalakumari NK, Piñeros M, Craft E, Rutzke MA, Danku J, Lahner B, Punshon T et al (2014) OPT3 is a phloem-specific iron transporter that is essential for systemic iron signaling and redistribution of iron and cadmium in Arabidopsis. Plant Cell 26:2249–2264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou B, Yao W, Wang S, Wang X, Jiang T (2014) The metallothionein gene, TaMT3, from Tamarix androssowii confers Cd2+ tolerance in tobacco. Int J Mol Sci 15:10398–10409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu YL, Pilon-Smits EA, Tarun AS, Weber SU, Jouanin L, Terry N (1999) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing gamma-glutamylcysteine synthetase. Plant Physiol 121:1169–1178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu YG, Williams PN, Meharg AA (2008) Exposure to inorganic arsenic from rice: a global health issue? Environ Pollut 154:169–171

    Article  CAS  PubMed  Google Scholar 

  • Zientara K, Wawrzyńska A, Lukomska J, López-Moya JR, Liszewska F, Assunção AGL, Aarts MGM, Sirko A (2009) Activity of the AtMRP3 promoter in transgenic Arabidopsis thaliana and Nicotiana tabacum plants is increased by cadmium, nickel, arsenic, cobalt and lead but not by zinc and iron. J Biotechnol 139:258–263

    Article  CAS  PubMed  Google Scholar 

  • Zimeri AM, Dhankher OP, McCaig B, Meagher RB (2005) The plant MT1 metallothioneins are stabilized by binding cadmiums and are required for cadmium tolerance and accumulation. Plant Mol Biol 58:839–855

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

A grant (MAS00401) to OPD from the US Department of Agriculture via the University of Massachusetts Amherst supported the writing of this manuscript.

Author information

Authors and Affiliations

  1. Stockbridge School of Agriculture, University of Massachusetts Amherst, Amherst, MA, 01002, USA

    Parul Rana Tomar & Om Parkash Dhankher

  2. John F. Kennedy Space Center, Merritt Island, FL, 32899, USA

    Anirudha R. Dixit

  3. Centre for Biotechnology, Maharishi Dayanand University, Rohtak, 124001, Haryana, India

    Pawan Kumar Jaiwal

Authors
  1. Parul Rana Tomar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anirudha R. Dixit
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pawan Kumar Jaiwal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Om Parkash Dhankher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Om Parkash Dhankher .

Editor information

Editors and Affiliations

  1. Center for Biotechnology, M.D. University, Rohtak, Haryana, India

    Pawan Kumar Jaiwal

  2. Department of Environmental Science, Babasaheb Bhimrao Ambedkar University, Lucknow, Uttar Pradesh, India

    Rana Pratap Singh

  3. Stockbridge School of Agriculture, University of Massachusetts Amherst, Amherst, Massachusetts, USA

    Om Parkash Dhankher

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer India

About this chapter

Cite this chapter

Tomar, P.R., Dixit, A.R., Jaiwal, P.K., Dhankher, O.P. (2015). Engineered Plants for Heavy Metals and Metalloids Tolerance. In: Jaiwal, P., Singh, R., Dhankher, O. (eds) Genetic Manipulation in Plants for Mitigation of Climate Change. Springer, New Delhi. https://doi.org/10.1007/978-81-322-2662-8_7

Download citation

Publish with us

Policies and ethics

Search

Navigation