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Proteomics of Plant Hyperaccumulators

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Metal Toxicity in Plants: Perception, Signaling and Remediation

Abstract

Plant metal hyperaccumulators take up and detoxify high concentrations of metal ions in their roots and shoots. They constitute an exceptional biological material for understanding mechanisms regulating plant metal homeostasis and plant adaptation to extreme environments. Hyperaccumulation physiology has recently also been studied with molecular tools. Indeed making use of transcriptome analysis it has been demonstrated that different expression patterns of genes accompanied different responses to metals between hyperaccumulator and non-hyperaccumulator plant species. The proteomic approach can also be powerful in dissecting the hyperaccumulator phenotype and the complex involvement of the protein regulation in this phenomenon. This chapter focuses on the recent developments in the application of proteomics to the analysis of hyperaccumulators providing a comprehensive review of key literature data of plant−metal − in particular Cd, Ni and Zn − hyperaccumulation.

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Abbreviations

2D-LC:

Two-dimensional liquid chromatography

2D-PAGE:

Two-dimensional polyacrylamide gel electrophoresis

APX:

Ascorbate peroxidase

ESI:

Electrospray ionization tandem mass spectrometry

GAPDH:

Glyceraldehyde-3-phosphate dehydrogenase

GST:

Glutathione S transferase

HS:

Heat-shock

IEF:

Isoelectric focusing

iTRAQs:

Isobaric Tag for Relative and Absolute Quantification

LC:

La Calamine

LE:

Lenninger

MALDI-TOF:

Matrix-assisted laser desorption/ionization time-of-flight

MP:

Monte Prinzera

MS:

Mass spectrometry

MudPIT:

Multidimensional protein identification technology

ROS:

Reactive oxygen species

RpR:

(Rožžnov pod Radhštěm-Moravia)

RuBisCo:

Ribulose 1,5-bisphosphate carboxylase/oxybenase

SOD:

Superoxide dismutase

References

  • Abou-Shanab RA, Angle JS, Delorme TA, Chaney RL, van Berkum P, Moawad H, Ghanem K, Ghozlan HA (2003a) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158:219–224

    Article  CAS  Google Scholar 

  • Abou-Shanab RI, Delorme TA, Angle JS, Chaney RL, Ghanem K, Moawad H, Ghozlan HA (2003b) Phenotypic characterization of microbes in the rhizosphere of Alyssum murale. Int J Phytoremediation 5:367–379

    PubMed  CAS  Google Scholar 

  • Abou-Shanab RAI, Angle JS, Chaney RL (2006) Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate and high Ni soils. Soil Biol Biochem 38:2882–2889

    Article  CAS  Google Scholar 

  • Ahsan N, Renaut J, Komatsu S (2010) Recent development in the application of proteomics to the analysis of plant responses to heavy metals. Proteomics 9:2602–2621

    Article  Google Scholar 

  • Alford ER, Pilon-Smits EAH, Paschke MW (2010) Metallophytes- A view from the rhizosphere. Plant Soil 337:33–50

    Article  CAS  Google Scholar 

  • Aloui A, Recorbet G, Gollotte A, Robert F, Valot B, Gianinazzi-Pearson V, Aschi-Smiti S, Dumas-Gaudot E (2009) On the mechanisms of cadmium stress alleviation in Medicago truncatula by Arbuscular mycorrhizal symbiosis: a root proteomic study. Proteomics 9:420–433

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Assunção AGL, Schat H, Aarts MGM (2003a) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159:411–419

    Article  Google Scholar 

  • Assunção AGL, Ten Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003b) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419

    Article  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 

  • Baker AJM, Ernst WHO, van der Ent A, Malaisse F, Ginocchio R (2010) Metallophytes: the unique biological resource, its ecology and conservational status in Europe, Central Africa and Latin America. In: Batty LC, Hallberg KB (eds) Ecology of industrial pollution. Cambridge University Press, Cambridge

    Google Scholar 

  • Basic N, Salamin N, Keller C, Gallard N, Besnard G (2006) Cadmium hyperaccumulatin and genetic differentiation of Thlaspi caerulescens populations. Biochem Syst Ecol 34:667–677

    Article  CAS  Google Scholar 

  • Bastida F, Moreno JL, Nicolas C, Hernandez T, Garcia C (2009) Soil metaproteomics: a review of an emerging environmental science. Significance, methodology and perspectives. Eur J Soil Sci 60:845–859

    Article  CAS  Google Scholar 

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

    Article  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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bona E, Cattaneo C, Cesaro P, Marsano F, Lingua G, Cavalletto M, Berta G (2010) Proteomic analysis of Pteris vittata fronds: two arbuscular fungi differentially modulate protein expression under arsenic contamination. Proteomics 10:811–3834

    Article  Google Scholar 

  • Boyd RS (2007) The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293:153–176

    Article  CAS  Google Scholar 

  • Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702

    Article  PubMed  CAS  Google Scholar 

  • Brooks RR, Lee J, Jaffré T (1974) Some New Zealand and New Caledonian plant accumulators of nickel. J Ecol 62:493–499

    Article  CAS  Google Scholar 

  • Brooks RR, Lee J, Reeves RD, Jaffré T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57

    Article  CAS  Google Scholar 

  • Brooks RR, Morrison RS, Reeves RD, Dudley TR, Akman Y (1979) Hyperaccumulation of nickel by Alyssum Linnaeus (Cruciferae). Proc R Soc Lond B 203:387–403

    Article  PubMed  CAS  Google Scholar 

  • Careri M, Mangia A (2011) Trends in analytical atomic and molecular mass spectrometry in biology and the life sciences. Anal Bioanal Chem 399:2585–2595

    Article  PubMed  CAS  Google Scholar 

  • Carpentier SC, Witters E, Laukens K, Deckers P, Swennen R, Panis B (2005) Preparation of protein extracts from recalcitrant plant tissues: an evaluation of different methods for two dimensional gel electrophoresis analysis. Proteomics 5:2497–2507

    Article  PubMed  CAS  Google Scholar 

  • Chaney R, Malik M, Li YM, Brown SL, Brewer EP, Angle JS, Baker AJM (1997) Phytoremediation of soil metals. Curr Opin Biotech 8:279–284

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Comerford NB (2005) Soil factors affecting nutrient bioavailability. In: BassiriRad H (ed) Nutrient acquisition by plants an ecological perspective. Springer, Heidelberg

    Google Scholar 

  • David JL, Zivy M, Cardin ML, Brabant P (1997) Protein evolution in dynamically managed populations of wheat: adaptative responses to macro-environmental conditions. Theor Appl Genet 95:932–941

    Article  CAS  Google Scholar 

  • Duquesnoy I, Goupil P, Nadaud I, Branlard G, Piquet-Pissaloux A, Ledoigt G (2009) Identification of Agrostis tenuis leaf proteins in response to As(V) and As(III) induced stress using a proteomics approach. Plant Sci 176:206–213

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ernst WHO (1996) Bioavailability of heavy metals and decontamination of soils by plants. Appl Geochem 11:163–167

    Article  CAS  Google Scholar 

  • Farinati S, DalCorso G, Bona E, Corbella M, Lampis S, Cecconi D, Polati R, Berta G, Vallini G (2009) A Proteomic analysis of Arabidopsis halleri shoots in response to the heavy metals cadmium and zinc and rhizosphere microorganisms. Proteomics 9:4837–4850

    Article  PubMed  CAS  Google Scholar 

  • Fraser JA, Davis MA, Hynes MJ (2002) A gene from Aspergillus nidulans with similarity to URE2 of Saccharomyces cerevisiae encodes a glutathione S-transferase which contributes to heavy metal and xenobiotic resistance. Appl Environ Microb 68:2802–2808

    Article  CAS  Google Scholar 

  • Freeman JL, Persans MW, Nieman K, Albrect 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  PubMed  CAS  Google Scholar 

  • Gegenhemier P (1990) Preparation of extracts from plants. Methods Enzymol 182:174–193

    Article  Google Scholar 

  • Giavalisco P, Nordhoff E, Lehrach H, Gobom J, Klose J (2003) Extraction of proteins from plant tissues for two-dimensional electrophoresis analysis. Electrophoresis 24:207–216

    Article  PubMed  CAS  Google Scholar 

  • Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19:1720–1730

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Krämer U (2008) Evolution of metal hyperaccumulation required cis regulatory changes and triplication of HMA4. Nature 453:391–395

    Article  PubMed  CAS  Google Scholar 

  • Hinsinger P (1998) How do plant roots acquire mineral nutrients? Chemical processes involved in the rhizosphere. In: Sparks DL (ed) Advances in agronomy, vol 64. Academic, San Diego

    Google Scholar 

  • Ingle RA, Smith JA, Sweetlove LJ (2005) Responses to nickel in the proteome of the hyperaccumulator plant Alyssum lesbiacum. Biometals 18:627–641

    Article  PubMed  CAS  Google Scholar 

  • Jacobs DI, van Rijssen MS, Heijden RVD, Verpoorte R (2001) Sequential solubilisation of proteins precipitated with trichloroacetic acid in acetone from cultured Catharanthus roseus cell yields 52% more spots after two dimensional electrophoresis. Proteomics 1:1345–1350

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Lambert JP, Ethier M, Smith JC, Figeys D (2005) Proteomics: from gel based to gel free. Anal Chem 77:3771–3788

    Article  PubMed  CAS  Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stresses. Academic, New York

    Google Scholar 

  • Li YM, Chaney R, Brewer E, Roseberg R, Angle JS, Baker A, Reeves R, Nelkin J (2003) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant Soil 249:107–115

    Article  CAS  Google Scholar 

  • Li WC, Ye ZH, Wong MH (2007) Effects of bacteria an enhanced metal uptake of the Cd/Zn-hyperaccumulating plant, Sedum alfredii. J Exp Bot 58:4173–4182

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Zhu YG, Chen BD, Christie P, Li XL (2005) Influence of the arbuscular mycorrhizal fungus Glomus mosseae on uptake of arsenate by the as hyperaccumulator fern Pteris vittata L. Mycorrhiza 15:187–192

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Christie P, Zhang JL, Li XL (2009) Growth and arsenic uptake by Chinese brake fern inoculated with an Arbuscular mycorrhizal fungus. Environ Exp Bot 66:435–441

    Article  CAS  Google Scholar 

  • 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 128:1359–1367

    Article  PubMed  CAS  Google Scholar 

  • Macnair MR (2003) The hyperaccumulation of metals by plants. Adv Bot Res 40:63–105

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Marmiroli N, McCutcheon SC (2003) Making phytoremediation a successful technology. In: McCutcheon SC, Schnoor JL (eds) Phytoremediation: transformation and control of contaminants. Wiley, Hoboken

    Google Scholar 

  • Memon AR, Schroeder P (2009) Implications of metal accumulation mechanisms to phytoremediation. Environ Sci Pollut R 16:162–175

    Article  CAS  Google Scholar 

  • Michaud D, Asselin A (1995) Application to plant proteins of gel electrophoretic methods. J Chromatogr A 698:263–279

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Moradi AB, Conesa HM, Robinson BH, Lehmann E, Kaestner A, Schulin R (2009) Root responses to soil Ni heterogeneity in a hyperaccumulator and a non-accumulator species. Environ Pollut 157:2189–2196

    Article  PubMed  CAS  Google Scholar 

  • Nesvizhskii AI (2007) Protein identification by tandem mass spectrometry and sequence database searching. Methods Mol Biol 367:87–119

    PubMed  CAS  Google Scholar 

  • Palmgren MG, Clemens S, Williams LE, Krämer U, Borg S, Schjørring JK, Sanders D (2008) Zinc biofortification of cereals: problems and solutions. Trends Plant Sci 13:464–473

    Article  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 U S A 97:4956–4960

    Article  PubMed  CAS  Google Scholar 

  • Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:5–39

    Article  Google Scholar 

  • Pirondini A, Visioli G, Malcevschi A, Marmiroli N (2006) A 2-D liquid–phase chromatography analysis in plant tissues. J Chromatogr B 833:91–100

    Article  CAS  Google Scholar 

  • Pollard AJ, Powell KD, Harper FA, Smith JAC (2002) The genetic basis of metal hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566

    Article  CAS  Google Scholar 

  • Poschenrieder C, Tolrà R, Barceló J (2006) Can metals defend plants against biotic stress? Trends Plant Sci 11:288–295

    Article  PubMed  CAS  Google Scholar 

  • Rabilloud T (1996) Solubilization of proteins for electrophoretic analyses. Electrophoresis 17:813–829

    Article  PubMed  CAS  Google Scholar 

  • Ramos-Onsins SE, Stranger BE, Mitchell-Olds T, Aguadé M (2004) Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata. Genetics 166:373–388

    Article  PubMed  CAS  Google Scholar 

  • Reeves RD (2003) Tropical hyperaccumulators of metals and their potential for phytoextraction. Plant Soil 249:57–65

    Article  CAS  Google Scholar 

  • Reeves RD (2006) Hyperaccumulation of trace elements by plants. In: Morel JL, Echevarria G, Goncharova N (eds) Phytoremediation of metal-contaminated soils. NATO science series: IV: earth and environmental sciences, Vol. 68 New York, NY, USA, Springer 1–25

    Google Scholar 

  • Reeves RD, Baker AJM (2000) Phytoremediation of toxic metals: using plants to clean up the environment. In: Raskin I, Ensley BD (eds) Metal accumulating plants. Wiley, New York

    Google Scholar 

  • Repetto O, Bestel-Corre G, Dumas-Gaudot E, Berta G, Gianinazzi-Pearson V, Gianinazzi S (2003) Targeted proteomics to identify cadmium-induced protein modifications in Glomus mosseae-inoculated pea roots. New Phytol 157:555–568

    Article  CAS  Google Scholar 

  • Richau KM, Schat H (2009) Intraspecific variation of nickel and zinc accumulation and tolerance in the hyperaccumulator Thlapsi caerulescens. Plant Soil 293:107–119

    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

    Article  PubMed  CAS  Google Scholar 

  • Rigola D, Fiers M, Vurro E, Aarts MGM (2006) The heavy metal hyperaccumulator Thlaspi caerulescens expresses many species-specific genes, as identified by comparative expressed sequence tag analysis. New Phytol 170:753–766

    Article  PubMed  CAS  Google Scholar 

  • Rose JKC, Bashir S, Giovannoni JJ, Jahn MM, Saravanan RS (2004) Tackling the plant proteome: practical approaches, hurdles and experimental tools. Plant J 39:715–733

    Article  PubMed  CAS  Google Scholar 

  • Rustichelli C, Visioli G, Kostecka D, Vurro E, Sanità di Toppi L, Marmiroli N (2008) Proteomic analysis in the lichen Physcia adscendens exposed to cadmium stress. Environ Pollut 156:1121–1127

    Article  PubMed  CAS  Google Scholar 

  • Sors TG, Ellis DR, Na GN, Lahner B, Lee S, Leustek T, Pickering IJ, Salt DE (2005) Analysis of sulfur and selenium assimilation in Astragalus plants with varying capacities to accumulate selenium. Plant J 42:785–797

    Article  PubMed  CAS  Google Scholar 

  • Trotta A, Falaschi P, Cornara L, Minganti V, Fusconi A, Drava G, Berta G (2006) Arbuscular mycorrhiza increase the arsenic translocation factor in the As hyperaccumulating fern Pteris vittata L. Chemosphere 65:74–81

    Article  PubMed  CAS  Google Scholar 

  • Tuomainen MH, Nunan N, Lehesranta SJ, Tervahauta AI, Hassinen VH, Schat H, Koistinen KM, Auriola S, McNicol J, Karenlampi S (2006) Multivariate analysis of protein profiles of metal hyperaccumulator Thlaspi caerulescens accessions. Proteomics 6:3696–3706

    Article  PubMed  CAS  Google Scholar 

  • Tuomainen M, Tervahauta A, Hassinen V, Schat H, Koistinen KM, Lehesranta S, Rantalainen K, Häyrinen J, Auriola S, Anttonen M, Kärenlampi S (2010) Proteomics of Thlapsi caerulescens accessions and an interaccession cross segregating for zinc accumulation. J Exp Bot 61:1075–1087

    Article  PubMed  CAS  Google Scholar 

  • Turnau K, Mesjasz-Przybylowicz J (2003) Arbuscular mycorrhiza of Berkheya coddii and other Ni-hyperaccumulating members of Asteraceae from ultramafic soils in South Africa. Mycorrhiza 13:185–190

    Article  PubMed  Google Scholar 

  • Valot B, Negroni L, Zivy M, Gianinazzi S, Dumas-Gaudot E (2006) A mass spectrometric approach to identify Arbuscular mycorrhiza-related proteins in root plasma membrane fractions. Proteomics 6:S145–S155

    Article  PubMed  Google Scholar 

  • van de Mortel JE, Almar Villanueva L, Schat H, Kwekkeboom J, Coughlan S, Perry D, Moerland PD, van Themaat EVL, 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

    Article  PubMed  Google Scholar 

  • van de Mortel JE, Schat H, Moerland PD, van Themaat EVL, 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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Vincent D, Wheatley DM, Cramer RG (2006) Optimization of protein extraction and solubilization for mature grape berry clusters. Electrophoresis 27:1853–1865

    Article  PubMed  CAS  Google Scholar 

  • Visioli G, Marmiroli M, Marmiroli N (2010a) Two dimensional liquid chromatography (2D-LC) technique coupled with mass spectrometry analysis to compare the proteomic response to Cd stress in plants. J Biomed Biotechnol 2010:1–10

    Article  Google Scholar 

  • Visioli G, Pirondini A, Malchevshi A, Marmiroli N (2010b) Comparison of proteomic variation in Thlaspi caerulescens populations from metalliferous and non metalliferous soils. Int J Phytoremediat 12:805–819

    Article  CAS  Google Scholar 

  • Vogel-Mikuš K, Pongrac P, Kump P, Nečemer M, Regvar M (2006) Colonisation of a Zn, Cd and Pb hyperaccumulator Thlaspi praecox Wulfen with indigenous Arbuscular mycorrhiza fungal mixture induces changes in heavy metal and nutrient uptake. Environ Pollut 139:362–371

    Article  PubMed  Google Scholar 

  • Walliwalagedara C, Atkinson I, van Keulen H, Cutright T, Wei R (2010) Differential expression of proteins induced by lead in the dwarf sunflower Helianthus annuus. Phytochemistry 71:1460–1465

    Article  PubMed  CAS  Google Scholar 

  • Waschke A, Sieh D, Tamasloukht M, Fischer K, Mann P, Franken P (2006) Identification of heavy metal-induced genes encoding glutathione S-transferases in the Arbuscular mycorrhira fungus Glomus intraradices. Mycorrhiza 17:1–10

    Article  PubMed  CAS  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 nicotinamine synthase, a ZIP transporter and other genes as potential hyperaccumulation factors. Plant J 37:269–281

    Article  PubMed  CAS  Google Scholar 

  • Whiting SN, De Souza MP, Terry N (2001) Rhizosphere bacteria mobilize Zn for hyperaccumulation by Thlaspi caerulescens. Environ Sci Technol 35:3144–3150

    Article  PubMed  CAS  Google Scholar 

  • Willems G, Drager DB, Courbot M, Gode 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

    Article  PubMed  CAS  Google Scholar 

  • Yang XE, Feng Y, He ZL, Stoffella PJ (2005) Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J Trace Elem Med Bio 18:339–353

    Article  CAS  Google Scholar 

  • Zeng XW, Qiu RL, Ying RR, Tang YT, Tang L, Fang XH (2011) The differentially-expressed proteome in Zn/Cd hyperaccumulator Arabis paniculata Franch. in response to Zn and Cd. Chemosphere 82:321–328

    Article  PubMed  CAS  Google Scholar 

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Visioli, G., Marmiroli, N. (2012). Proteomics of Plant Hyperaccumulators. 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_8

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