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Genetic and Molecular Aspects of Metal Tolerance and Hyperaccumulation

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Metal Toxicity in Plants: Perception, Signaling and Remediation

Abstract

Metals in the environment constitute a stress and a selective factor for plants, since they are genotoxic and toxic at high concentration. Plant responses to metals demonstrate the existence of different mechanisms for resistance, tolerance, accumulation and hyperaccumulation. This chapter analyses the most recent literature on the subject to highlight the different approaches which have been applied to elucidate the genetic and molecular bases of tolerance and accumulation. The data show that our knowledge of these events is not yet complete and that new research areas are needed.

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References

  • Arizi 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

    Google Scholar 

  • Arrivault S, Senger T, Kraemer U (2006) The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J 46:861–879

    PubMed  CAS  Google Scholar 

  • Assunçao AGL, Da Costa MP, de Folter S, Vooijs R, Schat H, Aarts MGM (2001) Elevated expression of metal transporter genes in three accesssons of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 24:217–226

    Google Scholar 

  • Assunçao AGL, Pieper B, Vromans J, Lindhout P, Aarts MG, Schat H (2006) Construction of a genetic linkage map of Thlaspi caerulescens and quantitative trait loci analysis of zinc accumulation. New Phytol 170:21–32

    PubMed  Google Scholar 

  • Assunção AGL, Ten Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003) A cosegregation analysis of zinc (Zn) accumulation and Zn tolerance in the Zn hyperaccumulator Thlaspi caerulescens. New Phytol 159:383–390

    Google Scholar 

  • Baker AJM (1987) Metal tolerance. New Phytol 106(Suppl s1):93–111

    CAS  Google Scholar 

  • Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements. A review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

    CAS  Google Scholar 

  • Becher M, Talke IN, Krall L, Kraemer 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

    PubMed  CAS  Google Scholar 

  • Bert V, Bonnin I, Saumitou-Laprade P, de Laguérie P, Petit D (2002) Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytol 155:47–57

    CAS  Google Scholar 

  • Bert V, Meerts P, Saumitou-Laprade P, Salis P, Gruber W, Verbruggen N (2003) Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri. Plant Soil 249:9–18

    CAS  Google Scholar 

  • Besnard G, Basic N, Christin P-A, Savova-Bianchi D, Galland N (2009) Thlaspi caerulescens (Brassicaceae) population genetics in western Switzerland: is the genetic structure affected by natural variation of soil heavy metal concentration? New Phytol 181:974–984

    PubMed  CAS  Google Scholar 

  • Bovet L, Kammer PM, Meylan-Bettex M, Guadagnuolo R, Matera V (2006) Cadmium accumulation capacities of Arabis alpina under environmental conditions. Environ Exp Bot 57:80–88

    CAS  Google Scholar 

  • Broadley MR, Willey NJ, Wilkins JC, Baker AJM, Mead A, White PJ (2001) Phylogenetic variation in heavy metal accumulation in angiosperms. New Phytol 152:9–27

    CAS  Google Scholar 

  • Chiang HC, Lo JC, Yeh KC (2006) Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environ Sci Technol 40:6792–6798

    PubMed  CAS  Google Scholar 

  • Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719

    PubMed  CAS  Google Scholar 

  • Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, Saumitou-Laprade P, Verbruggen N (2007) A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol 144:1052–1065

    PubMed  CAS  Google Scholar 

  • Couselo JL, Navarro-Avino J, Ballester A (2010) Expression of the phytochelatin synthase TaPCS1 in transgenic aspen, insight into the problems and qualities in phytoremediation of Pb. Int J Phytoremediation 12:358–370

    PubMed  CAS  Google Scholar 

  • Deniau AX, Pieper B, Ten Bookum WM, Lindhout P, Aarts MG, Schat H (2006) QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens. Theor Appl Genet 113:907–920

    PubMed  CAS  Google Scholar 

  • Draeger DB, Desbrosses-Fonrouge A-G, Krach C, Chardonnens AN, Meyer RC, Saumitou-Laprade P, Kraemer 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

    CAS  Google Scholar 

  • Ernst WHO, Krauss GJ, Verkleij JAC, Wesenberg D (2008) Interaction of heavy metals with the sulphur metabolism in angiosperms from an ecological point of view. Plant Cell Environ 31:123–143

    PubMed  CAS  Google Scholar 

  • Filatov V, Dowdle J, Smirnoff N, Ford-Lloyd B, Newbury HJ, Macnair M (2006) Comparison of gene expression in segregating families identifies genes and genomic regions involved in a novel adaptation, zinc hyperaccumulation. Mol Ecol 15:3045–3059

    PubMed  CAS  Google Scholar 

  • Filatov V, Dowdle J, Smirnoff N, Ford-Lloyd B, Newbury HJ, Macnair M (2007) A quantitative trait loci analysis of zinc hyperaccumulation in Arabidopsis halleri. New Phytol 174:580–590

    PubMed  CAS  Google Scholar 

  • Fones H, Davis CAR, Rico A, Fang F, Smith JAC, Preston GM (2010) Metal hyperaccumulation armors plants against disease. PLoS Pathog 6(9):e1001093

    PubMed  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

    PubMed  CAS  Google Scholar 

  • Frérot H, Petit C, Lefèbvre C, Gruber W, Collin C, Escarré J (2003) Zinc and cadmium accumulation in controlled crosses between metallicolous and nonmetallicolous populations of Thlaspi caerulescens (Brassicaceae). New Phytol 157:643–648

    Google Scholar 

  • Fusco N, Micheletto L, Dal Corso G, Borgato L, Furini A (2005) Identification of cadmium-regulated genes by cDNA-AFLP in the heavy metal accumulator Brassica juncea L. J Exp Bot 56:3017–3027

    PubMed  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 USA 95:7220–7224

    PubMed  CAS  Google Scholar 

  • Gullì M, Rampino P, Lupotto E, Marmiroli N, Perrotta C (2005) The effect of heat stress and cadmium ions on the expression of a small hsp gene in barley and maize. J Cereal Sci 42:25–31

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Guo W-J, Meetam M, Goldsbrough PB (2008b) Examining the specific contribution of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiol 146:1697–1706

    PubMed  CAS  Google Scholar 

  • 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 57:1116–1127

    PubMed  CAS  Google Scholar 

  • Ha S-B, Smith AP, Howden R, Dietrich WM, Bugg S, O’Connell MJ, Goldsbrough PB, Cobbett CS (1999) Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11:1153–1164

    PubMed  CAS  Google Scholar 

  • Hammond JP, Bowen HC, White PJ, Mills V, Pyke KA, Baker AJM, Whiting SN, May ST, Broadley MR (2006) A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol 170:239–260

    PubMed  CAS  Google Scholar 

  • Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Kraemer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–396

    PubMed  CAS  Google Scholar 

  • Hartwig A (1998) Carcinogenicity of metal compounds: possible role of DNA repair inhibition. Toxicol Lett 102–103:235–239

    PubMed  Google Scholar 

  • Hashiguchi A, Ahsan N, Komatsu S (2010) Proteomics application of crops in the context of climatic changes. Food Res Int 43:1803–1813

    CAS  Google Scholar 

  • Hassinen VH, Tervahauta AI, Halimaa P, Plessl M, Peraniemi S, Schat H, Aarts MGM, Servomaa K, Karenlampi SO (2007) Isolation of Zn-responsive genes from two accessions of the hyperaccumulator plant Thlaspi caerulescens. Planta 225:977–989

    PubMed  CAS  Google Scholar 

  • Hassinen VH, Tuomainen M, Peraniemi S, Schat H, Karenlampi SO, Tervahauta AI (2009) Metallothioneins 2 and 3 contribute to the metal-adapted phenotype but are not directly linked to Zn accumulation in the metal hyperaccumulator, Thlaspi caerulescens. J Exp Bot 6:187–196

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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 17:2089–2106

    PubMed  CAS  Google Scholar 

  • Ishimaru Y, Masuda H, Suzuki M, Bashir K, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2007) Overexpression of the OsZIP4 zinc transporter confer disarrangement of zinc distribution in rice plants. J Exp Bot 58:2909–2915

    PubMed  CAS  Google Scholar 

  • Kawashima CG, Noji M, Nakamura M, Ogra Y, Suzuki KT, Saito K (2004) Heavy metal tolerance of transgenic tobacco plants over-expressing cysteine synthase. Biotechnol Lett 26:153–157

    PubMed  CAS  Google Scholar 

  • Kim S, Takahashi M, Higuchi K, Tsunoda K, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2005) Increased nicotianamine biosynthesis confers enhanced tolerance of high levels of metals, in particular nickel, to plants. Plant Cell Physiol 46:1809–1818

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Koch M, Mummenhoff K, Hurka H (1998) Systematics and evolutionary history of heavy metal tolerant Thlaspi caerulescens in Western Europe: evidence from genetic studies based on isozyme analysis. Biochem Syst Ecol 26:823–838

    CAS  Google Scholar 

  • Korenkov V, Hirschi K, Crutchfield JD, Wagner GJ (2007) Enhancing tonoplast Cd/H antiport activity increases Cd, Zn, and Mn tolerance, and impacts root/shoot Cd partitioning in Nicotiana tabacum L. Planta 226:1379–1387

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Kraemer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534

    CAS  Google Scholar 

  • Kraemer 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

    Google Scholar 

  • LeDuc DL, Tarun AS, Montes-Bayon M, Meija J, Malit MF, Wu CP, AbdelSamie M, Chiang C-Y, Tagmount A, deSouza M, Neuhierl B, Boeck A, Caruso J, Terry N (2004) Overexpression of selenocysteine methyltransferase in Arabidopsis and indian mustard increases selenium tolerance and accumulation. Plant Physiol 135:377–383

    PubMed  CAS  Google Scholar 

  • Macnair MR (2002) Within and between population genetic variation for zinc accumulation in Arabidopsis halleri. New Phytol 155:59–66

    CAS  Google Scholar 

  • Macnair MR, Bert V, Huitson SB, Saumitou-Laprade P, Petit D (1999) Zinc tolerance and hyperaccumulation are genetically independent characters. Proc Biol Sci 266:2175–2179

    PubMed  CAS  Google Scholar 

  • Maestri E, Marmiroli N (2011) Transgenic plants for phytoremediation. Int J Phytorem 1 First published on 4 April 2011 (First). doi:10.1080/15226514.2011.568549

  • Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13

    CAS  Google Scholar 

  • Maksymiec W (2007) Signaling responses in plants to heavy metal stress. Acta Physiol Plant 29:177–187

    CAS  Google Scholar 

  • Marmiroli N, Maestri E (2008) Health implications of trace elements in the environment and the food chain. In: Prasad MNV (ed) Trace elements as contaminants and nutrients: consequences in ecosystems and human health. Wiley, New York

    Google Scholar 

  • Marmiroli N, Restivo FM, Smith CJ, Di Cola G, Maestri E, Tassi F (1997) Induction of heat shock response and acquisition of thermotolerance in callus cultures of Gerbera jamesonii. In Vitro Cell Dev Biol Plant 33:49–55

    CAS  Google Scholar 

  • Marmiroli M, Visioli G, Antonioli G, Maestri E, Marmiroli N (2009) Integration of XAS techniques and genetic methodologies to explore Cs-tolerance in Arabidopsis. Biochimie 91:180–191

    PubMed  CAS  Google Scholar 

  • McDiarmid CW, Milanick MA, Eide DJ (2003) Induction of the ZRC1 metal tolerance gene in zinc-limited yeast confers resistance to zinc shock. J Biol Chem 278:15065–15072

    Google Scholar 

  • Meerts P, Van Isacker N (1997) Heavy metal tolerance and accumulation in metallicolous and non-metallicolous populations of Thlaspi caerulescens from continental Europe. Plant Ecol 133:221–231

    Google Scholar 

  • Mengoni A, Gonnelli C, Galardi F, Gabbrielli R, Bazzicalupo M (2000) Genetic diversity and heavy metal tolerance in populations of Silene paradoxa L. (Caryophyllaceae): a random amplified polymorphic DNA analysis. Mol Ecol 9:1319–1324

    PubMed  CAS  Google Scholar 

  • Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13

    PubMed  CAS  Google Scholar 

  • Mirouze M, Sels J, Richard O, Czernic P, Loubet S, Jacquier A, François IEJA, Cammue BPA, Lebrun M, Berthomieu P, Marques L (2006) A putative novel role for plant defensins: a defensin from the zinc hyper-accumulating plant, Arabidopsis halleri, confers zinc tolerance. Plant J 47:329–342

    PubMed  CAS  Google Scholar 

  • Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H (2011) OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189:190–199

    PubMed  CAS  Google Scholar 

  • O Lochlainn SO, Bowen HC, Fray RG, Hammond JP, King GJ, White PJ, Graham NS, Broadley MR (2011) Tandem quadruplication of HMA4 in the zinc (Zn) and casmium (Cd) hyperaccumulator Noccaea caerulescens. PLoS One 6(3):e17814

    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

    PubMed  CAS  Google Scholar 

  • Pauwels M, Roosens N, Frérot H, Saumitou-Laprade P (2008) When population genetics serves genomics: putting adaptation back in a spatial and historical context. Curr Opin Plant Biol 11:129–134

    PubMed  CAS  Google Scholar 

  • Pence NS, Larsen PB, Ebbs SD, Letham DLD, 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 USA 97:4956–4960

    PubMed  CAS  Google Scholar 

  • Persans MW, Nieman K, Salt DE (2001) Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proc Natl Acad Sci USA 98:9995–10000

    PubMed  CAS  Google Scholar 

  • Pianelli K, Mari S, Marques L, Lebrun M, Czernic P (2005) Nicotianamine over-accumulation confers resistance to nickel in Arabidopsis thaliana. Transgenic Res 14:739–748

    PubMed  CAS  Google Scholar 

  • Pilon-Smits EAH, Hwang SB, Lytle CM, Zhu YL, Tai JC, Bravo RC, Leustek T, Terry N (1999) Overexpression of ATP sulfurylase in Brassica juncea leads to increased selenate uptake, reduction and tolerance. Plant Physiol 119:123–132

    PubMed  CAS  Google Scholar 

  • Plaza S, Tearall KL, Zhao F-J, 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 58:1717–1728

    PubMed  CAS  Google Scholar 

  • Plessl M, Rigola D, Hassinen V, Aarts MGM, Schat H, Ernst D (2005) Transcription profiling of the metal-hyperaccumulator Thlaspi caerulescens (J & C PRESL). Z Naturforsch C 60:216–223

    PubMed  CAS  Google Scholar 

  • Rausch T, Gromes R, Liedschulte V, Mueller I, Bogs J, Galovic V, Wachter A (2007) Novel insight into the regulation of GSH biosynthesis in higher plants. Plant Biol 9:565–572

    PubMed  CAS  Google Scholar 

  • Richau KH, Schat H (2009) Intraspecific variation of nickel and zinc accumulation and tolerance in the hyperaccumulator Thlaspi caerulescens. Plant Soil 314:253–262

    CAS  Google Scholar 

  • Richau KH, Kozhevnikova AD, Seregin IV, Vooijs R, Koevoets PLM, Smith JAC, Ivanov VB, Schat H (2009) Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens. New Phytol 183:106–116

    PubMed  CAS  Google Scholar 

  • Roosens NHCJ, Willems G, Saumitou-Laprade P (2008a) Using Arabidopsis to explore zinc tolerance and hyperaccumulation. Trends Plant Sci 13:208–215

    PubMed  CAS  Google Scholar 

  • Roosens NHCJ, Willems G, Godé C, Courseaux A, Saumitou-Laprade P (2008b) The use of comparative genome analysis and syntenic relationships allows extrapolating the position of Zn tolerance QTL regions from Arabidopsis halleri into Arabidopsis thaliana. Plant Soil 306:105–116

    CAS  Google Scholar 

  • Sanjaya HPY, Su RC, Ko SS, Tong CG, Yang RY, Chan MT (2008) Overexpression of Arabidopsis thaliana tryptophan synthase beta 1 (AtTSB1) in Arabidopsis and tomato confers tolerance to cadmium stress. Plant Cell Environ 31:1074–1085

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Shahzad Z, Gosti F, Frérot H, Lacombe E, Roosens N, Saumitou-Laprade P, Berthomieu P (2010) The five AhMTP1 zinc transporters undergo different evolutionary fates towards adaptive evolution to zinc tolerance in Arabidopsis halleri. PLoS Genet 6(4):e1000911

    PubMed  Google Scholar 

  • Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK (2006) Transgenic tobacco overexpressing glyoxalase pathway enzymes grow and set viable seeds in zinc-spiked soils. Plant Physiol 140:613–623

    PubMed  CAS  Google Scholar 

  • Sinibaldi RM, Mettler IJ (1992) Intron splicing and intron-mediated enhanced expression in monocots. In: Cohn WE, Moldave K (eds) Progress in nucleic acid research and molecular biology. Academic, New York, pp 227–259

    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

    PubMed  CAS  Google Scholar 

  • Suzuki N, Koizumi N, Sano H (2001) Screening of cadmium-responsive genes in Arabidopsis thaliana. Plant Cell Environ 24:1177–1188

    CAS  Google Scholar 

  • Talke IN, Hanikenne M, Kraemer 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 142:148–167

    PubMed  CAS  Google Scholar 

  • Taylor SI, Macnair MR (2006) Within and between population variation for zinc and nickel accumulation in two species of Thlaspi (Brassicaceae). New Phytol 169:505–514

    PubMed  CAS  Google Scholar 

  • Tolrà R, Pongrac P, Poschenrieder C, Vogel-Mikus K, Regvar M, Barcelo J (2006) Distinctive effects of cadmium on glucosinolate profiles in Cd hyperaccumulator Thlaspi praecox and non-hyperaccumulator Thlaspi arvense. Plant Soil 288:333–341

    Google Scholar 

  • Urano K, Kurihara Y, Seki M, Shinozaki K (2010) ‘Omics’ analyses of regulatory networks in plant abiotic stress responses. Curr Opin Plant Biol 13:132–138

    PubMed  CAS  Google Scholar 

  • van de Mortel JE, Villanueva LA, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, ver Loren van Themaat E, Koornneef M, Aarts MGM (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147

    PubMed  Google Scholar 

  • van de Mortel JE, Schat H, Moerland PD, ver Loren van Themaat E, van der Ent S, Blankestijn H, Ghandilyan A, Tsiatsiani S, Aarts MGM (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 31:301–324

    PubMed  Google Scholar 

  • van der Zaal BJ, Neuteboom LW, Pinas JE, Chardonnens AN, Schat H, Verkleij JAC, Hooykaas PJJ (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 119:1047–1056

    PubMed  Google Scholar 

  • van Hoewyk D, Garifullina GF, Ackley AR, Abdel-Ghany SE, Marcus MA, Fakra S, Ishiyama K, Inoue E, Pilon M, Takahashi H, Pilon-Smits EAH (2005) Overexpression of AtCpNifS enhances selenium tolerance and accumulation in Arabidopsis. Plant Physiol 139:1518–1528

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776

    PubMed  CAS  Google Scholar 

  • Verkleij JAC, Golan-Goldhirsh A, Antosiewisz DM, Schwitzguébel J-P, Schröder P (2009) Dualities in plant tolerance to pollutants and their uptake and translocation to the upper plant parts. Environ Exp Bot 67:10–22

    CAS  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

    PubMed  CAS  Google Scholar 

  • Vielle-Calzada J-P, Martínez de la Vega O, Hernández-Guzmán G, Ibarra-Laclette E, Alvarez-Mejía C, Vega-Arreguín JC, Jiménez-Moraila B, Fernández-Cortés A, Corona-Armenta G, Herrera-Estrella L, Herrera-Estrella A (2009) The Palomero genome suggests metal effects on domestication. Science 326:1078

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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 37:269–281

    PubMed  CAS  Google Scholar 

  • Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2 + −hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 29:950–963

    PubMed  CAS  Google Scholar 

  • Wei W, Chai T, Zhang Y, Han L, Xu J, Guan Z (2009) The Thlaspi caerulescens NRAMP homologue TcNRAMP3 is capable of divalent cation transport. Mol Biotechnol 41:15–21

    PubMed  CAS  Google Scholar 

  • Willems G, Draeger DB, Courbot M, Godé C, Verbruggen N, Saumitou-Laprade P (2007) The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): an analysis of quantitative trait loci. Genetics 176:659–674

    PubMed  CAS  Google Scholar 

  • Wojas S, Hennin J, Plaza S, Geisler M, Siemianowski O, Sklodowska A, Ruszczynska A, Bulska E, Antosiewicz DM (2009) Ectopic expression of Arabidopsis ABC transporter MRP7 modifies cadmium root-to-shoot transport and accumulation. Environ Poll 157:2781–2789

    CAS  Google Scholar 

  • Wojas S, Clemens S, Sklodowska A, Antosiewicz DM (2010) Arsenic response of AtPCS1- and CePCS-expressing plants–effects of external as(V) concentration on as-accumulation pattern and NPT metabolism. J Plant Physiol 167:169–175

    PubMed  CAS  Google Scholar 

  • Wong CKW, Cobbett CS (2009) HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181:71–78

    PubMed  CAS  Google Scholar 

  • Xiong J, Fu G, Tao L, Zhu C (2010) Roles of nitric oxide in alleviating heavy metal toxicity in plants. Arch Biochem Biophys 497:13–20

    PubMed  CAS  Google Scholar 

  • Zha HG, Jiang RF, Zhao FJ, Vooijs R, Schat H, Barker JHA, McGrath SP (2004) Co-segregation analysis of cadmium and zinc accumulation in Thlaspi caerulescens interecotypic crosses. New Phytol 163:299–312

    CAS  Google Scholar 

  • Zhang Y, Wang Z, Chai T, Wen Z, Zhang H (2008) Indian mustard aquaporin improves drought and heavy-metal resistance in tobacco. Mol Biotechnol 40:280–292

    PubMed  CAS  Google Scholar 

  • Zhao C, Qiao M, Yu Y, Xia G, Xiang F (2010) The effect of the heterologous expression of Phragmites australis γ-glutamylcysteine synthetase on the Cd2+ accumulation of Agrostis palustris. Plant Cell Environ 22:877–887

    Google Scholar 

  • Zhigang A, Cuijie L, Yuangang Z, Yejie D, Wachter A, Gromes R, Rausch T (2006) Expression of BjMT2, a metallothionein 2 from Brassica juncea, increases copper and cadmium tolerance in Escherichia coli and Arabidopsis thaliana, but inhibits root elongation in Arabidopsis thaliana seedlings. J Exp Bot 57:3575–3582

    PubMed  Google Scholar 

  • Zientara K, Wawrzynska A, Lukomska J, Lopez-Moya JR, Liszewska F, Assunçao 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

    PubMed  CAS  Google Scholar 

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Acknowledgments

We thank the authors of papers and reviews cited in the chapter, and apologise to the authors who have not been cited due to space constraints. We acknowledge financial support by PRIN contracts (Italian Ministry of University). We thank Prof. Nelson Marmiroli for critical reading of the manuscript and helpful suggestions.

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Authors and Affiliations

  1. Department of Environmental Sciences, University of Parma, Parma, Italy

    Elena Maestri & Marta Marmiroli

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  1. Elena Maestri
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  2. Marta Marmiroli
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Correspondence to Elena Maestri .

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  1. CSIC, Bioquímica, Estación Experimental Del Zaidín, Apartado 419, Granada, E-18008, Spain

    Dharmendra K. Gupta

  2. CSIC, Bioquímica, Estación Experimental Del Zaidín, Apartado 419, Granada, E-18080, Spain

    Luisa M. Sandalio

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Maestri, E., Marmiroli, M. (2012). Genetic and Molecular Aspects of Metal Tolerance and Hyperaccumulation. In: Gupta, D., Sandalio, L. (eds) Metal Toxicity in Plants: Perception, Signaling and Remediation. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-22081-4_3

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