Advertisement

Biochemical and Functional Responses of Arabidopsis thaliana Exposed to Cadmium, Copper and Zinc

Chapter
Part of the Environmental Pollution book series (EPOL, volume 21)

Abstract

Phytoremediation has been accepted advantageous over commonly used civil engineering remediation methods in costs, practice and the scale at which the processes operate. Understanding the metabolic answer and the adaptation of plants towards toxic metal exposure opens the way to future phytoremediation of contaminated sites. The majority of these metals get accumulated in plants and may either directly or indirectly find their way into the food chain causing severe secondary consequences. In particular, excess cadmium (Cd), copper (Cu) and zinc (Zn) are known to induce stress effects in all plant species. However, while Cu and Zn are normally present in different soils, and are part of or act as cofactors of many cell macromolecules, plants have no metabolic requirement for Cd. Arabidopsis thaliana L. is considered a model plant for many studies as its genomic sequence was completely identified and its mechanisms in genomic, transcriptomic and proteomic regulation are often similar to other plant species. The molecular, biochemical, physiological and morphological characteristics of this species are strongly affected by the exposure to Cd, Cu and Zn. The aim of this work is to give an up-to-date overview on the recent breakthroughs in the area of responses and adaptation of A. thaliana to Cd, Cu and Zn, three of the most common metals found in polluted soils, both alone and in combination. This chapter aims to contribute to a better understanding of the fundamental aspects of detoxification of metals and general responses in phytoremediation. The numerous and easily available genetic resources developed in A. thaliana should be extended to fast growing plant species of high biomass having significant tolerance to metals and suitable for phytoremediation purposes.

Keywords

Arabidopsis thaliana L. Cadmium Copper Metals Multi-pollution Phytoremediation Zinc 

Abbreviations

Cd

Cadmium

CKs

Cytokinins

Cu

Copper

GSH

Reduced glutathione

IAA

Indole-3-acetic acid

MTs

Metallothioneins

PCS

Phytochelatin synthase

PCs

Phytochelatins

Zn

Zinc

References

  1. Abdel-Ghany SE, Muüller-Moulé P, Niyogi KK, Pilon M, Shikanai T (2005) Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17:1233–1251CrossRefGoogle Scholar
  2. Ager FJ, Ynsa MD, Domínguez-Solís JR, Gotor C, Respaldiza MA, Romero LC (2002) Cadmium localization and quantification in the plant Arabidopsis thaliana using micro-PIXE. Nucl Instrum Method B 189:494–498CrossRefGoogle Scholar
  3. Ager FJ, Ynsa MD, Domínguez-Solís JR, López-Martín MC, Gotor C, Romero LC (2003) Nuclear micro-probe analysis of Arabidopsis thaliana leaves. Nucl Instrum Method B 210:401–406CrossRefGoogle Scholar
  4. Arteca RN, Arteca JM (2007) Heavy-metal-induced ethylene production in Arabidopsis thaliana. J Plant Physiol 164:1480–1488CrossRefGoogle Scholar
  5. Barroso C, Romero LC, Cejudo FJ, Vega JM, Gotor C (1999) Salt-specific regulation of the cytosolic O-acetylserine(thiol)lyase gene from Arabidopsis thaliana is dependent on abscisic acid. Plant Mol Biol 40:729–736CrossRefGoogle Scholar
  6. Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L et al (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315CrossRefGoogle Scholar
  7. 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 96:6808–6813CrossRefGoogle Scholar
  8. Blum R, Meyer KC, Wünschmann J, Lendzian KJ, Grill E (2010) Cytosolic action of phytochelatin synthase. Plant Physiol 153:159–169CrossRefGoogle Scholar
  9. Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171CrossRefGoogle Scholar
  10. Cazalé A-C, Clemens S (2001) Arabidopsis thaliana expresses a second functional phytochelatin synthase. FEBS Lett 507:215–219CrossRefGoogle Scholar
  11. Chen A, Komives EA, Schroeder JI (2006) An improved grafting technique for mature Arabidopsis plants demonstrates long-distance shoot-to-root transport of phytochelatins in Arabidopsis. Plant Physiol 141:108–120CrossRefGoogle Scholar
  12. Clauss MJ, Koch MA (2006) Poorly known relatives of Arabidopsis thaliana. Trends Plant Sci 11:449–459CrossRefGoogle Scholar
  13. Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832CrossRefGoogle Scholar
  14. Cobbett CS (2003a) Metallothioneins and phytochelatins; the sulfur-containing, metal-binding ligands of plants. In: Abrol YP, Ahmad A (eds) Sulphur in plants. Kluwer Academic Publishers, Dordrecht, pp 177–188Google Scholar
  15. Cobbett CS (2003b) Metals and plants. Model systems and hyper-accumulator species. New Phytol 159:289–293CrossRefGoogle Scholar
  16. Cobbett CS, Meagher RB (2002) Arabidopsis and the genetic potential for the phytoremediation of toxic elemental and organic pollutants. In: Somerville CR, Meyerowitz EM (eds) The arabidopsis book. American Society of Plant Biologists, Rockville, http://www.aspb.org/publications/arabidopsis/ - this publication is only available as an on-line textGoogle Scholar
  17. 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 144:1052–1065CrossRefGoogle Scholar
  18. Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H, Opdenakker K et al (2010) Cadmium stress: an oxidative challenge. Biometals 23:927–940CrossRefGoogle Scholar
  19. Desbrosses-Fonrouge A-G, Voigt K, Schröder A, Arrivault S, Thomine S, Krämer U (2005) Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Lett 579:4165–4174CrossRefGoogle Scholar
  20. Domínguez-Solís JR, Gutiérrez-Alcalá G, Romero LC, Gotor C (2001) The cytosolic O-acetylserine(thiol)lyase gene is regulated by heavy metals and can function in cadmium tolerance. J Biol Chem 276:9297–9302CrossRefGoogle Scholar
  21. Dutilleul C, Jourdain A, Bourguignon J, Hugouvieux V (2008) The Arabidopsis putative selenium-binding protein family: expression study and characterization of SBP1 as a potential new player in cadmium detoxification processes. Plant Physiol 147:239–251CrossRefGoogle Scholar
  22. Duy D, Wanner G, Meda AR, von Wirén N, Soll J, Philippar K (2007) PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19:986–1006CrossRefGoogle Scholar
  23. Eren E, Argüello JM (2004) Arabidopsis HMA2, a divalent heavy metal-transporting PIB-type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol 136:3712–3723CrossRefGoogle Scholar
  24. Fukao Y, Ferjani A, Fujiwara M, Nishimori Y, Ohtsu I (2009) Identification of zinc-responsive proteins in the roots of Arabidopsis thaliana using a highly improved method of two-dimensional electrophoresis. Plant Cell Physiol 50:2234–2239CrossRefGoogle Scholar
  25. Gasic K, Korban SS (2007) Expression of Arabidopsis phytochelatin synthase in Indian mustard (Brassica juncea) plants enhances tolerance for Cd and Zn. Planta 225:1277–1285CrossRefGoogle Scholar
  26. Gojon A, Gaymard F (2010) Keeping nitrate in the roots: an unexpected requirement for cadmium tolerance in plants. J Mol Cell Biol 2:299–301CrossRefGoogle Scholar
  27. Gong J-M, Lee DA, Schroeder JI (2003) Long-distance root-to-shoot transport of phytochelatins and cadmium in Arabidopsis. Proc Natl Acad Sci U S A 100:10118–10123CrossRefGoogle Scholar
  28. Goodwin SB, Sutter TR (2009) Microarray analysis of Arabidopsis genome response to aluminum stress. Biol Plant 53:85–99CrossRefGoogle Scholar
  29. Guo W-J, Meetam M, Goldsbrough PB (2008) Examining the specific contributions of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiol 146:1697–1706CrossRefGoogle Scholar
  30. Hansen BG, Halkier BA (2005) New insight into the biosynthesis and regulation of indole compounds in Arabidopsis thaliana. Planta 221:603–606CrossRefGoogle Scholar
  31. Harada E, Yamaguchi Y, Koizumi N, Sano H (2002) Cadmium stress induces production of thiol compounds and transcripts for enzymes involved in sulfur assimilation pathways in Arabidopsis. J Plant Physiol 159:445–448CrossRefGoogle Scholar
  32. Hassinen VH, Tervahauta AI, Kärenlampi SO (2007) Searching for genes involved in metal tolerance, uptake, and transport. In: Willey N (ed) Phytoremediation. Methods and reviews. Humana Press Inc., Totowa, pp 265–289CrossRefGoogle Scholar
  33. Haydon MJ, Cobbett CS (2007) A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis thaliana. Plant Physiol 143:1705–1719CrossRefGoogle Scholar
  34. Herbette S, Taconnat L, Hugouvieux V, Piette L, Magniette M-LM, Cuine S, Auroy P, Richaud P, Forestier C et al (2006) Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88:1751–1765CrossRefGoogle Scholar
  35. Hirayama T, Kieber JJ, Hirayama N, Kogan M, Guzman P, Nourizadeh S, Alonso JM, Dailey WP, Dancis A, Ecker JR (1999) RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97:383–393CrossRefGoogle Scholar
  36. Howarth JR, Domínguez-Solís JR, Gutíerrez-Alcalá G, Wray JL, Romero LC, Gotor C (2003) The serine acetyltransferase gene family in Arabidopsis thaliana and the regulation of its expression by cadmium. Plant Mol Biol 51:589–598CrossRefGoogle Scholar
  37. Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, Young J, Camakaris J et al (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339CrossRefGoogle Scholar
  38. Kabata-Pendias A, Mukherjee AB (2007) Trace elements from soil to human. Springer, BerlinCrossRefGoogle Scholar
  39. Kai K, Horita J, Wakasa K, Miyagawa H (2007) Three oxidative metabolites of indole-3-acetic acid from Arabidopsis thaliana. Phytochemistry 68:1651–1663CrossRefGoogle Scholar
  40. Kanter U, Hauser A, Michalke B, Dräxl S, Schäffner AR (2010) Caesium and strontium accumulation in shoots of Arabidopsis thaliana: genetic and physiological aspects. J Exp Bot 61:3995–4009CrossRefGoogle Scholar
  41. Kashem MA, Singh BR, Kubota H, Sugawara R, Kitajima N, Kondo T, Kawai S (2010) Zinc tolerance and uptake by Arabidopsis halleri ssp. gemmifera grown in nutrient solution. Environ Sci Pollut Res Int 17:1174–1176CrossRefGoogle Scholar
  42. Kim D-Y, Bovet L, Kushnir S, Noh EW, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140:922–932CrossRefGoogle Scholar
  43. 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 40:37–44CrossRefGoogle Scholar
  44. Kung C-CS Huang W-N, Huang Y-C, Yeh K-C (2006) Proteomic survey of copper-binding proteins in Arabidopsis roots by immobilized metal affinity chromatography and mass spectrometry. Proteomics 6:2746–2758CrossRefGoogle Scholar
  45. Kvesitadze G, Khatisashvili G, Sadunishvili T, Ramsden JJ (eds) (2006) Biochemical mechanisms of detoxification in higher plants. Springer, BerlinGoogle Scholar
  46. Lee S, Moon JS, Ko T-S, Petros D, Goldsbrough PB, Korban SS (2003a) Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiol 131:656–663CrossRefGoogle Scholar
  47. Lee S, Petros D, Moon JS, Ko T-S, Goldsbrough PB, Korban SS (2003b) Higher levels of ectopic expression of Arabidopsis phytochelatin synthase do not lead to increased cadmium tolerance and accumulation. Plant Physiol Biochem 41:903–910CrossRefGoogle Scholar
  48. Li W, Khan MA, Yamaguchi S, Kamiya Y (2005) Effects of heavy metals on seed germination and early seedling growth of Arabidopsis thaliana. J Plant Growth Regul 46:45–50CrossRefGoogle Scholar
  49. Li Y, Dankher OP, Carreira L, Smith AP, Meagher RP (2006) The shoot-specific expression of γ-glutamylcysteine synthetase directs the long-distance transport of thiol-peptides to roots conferring tolerance to mercury and arsenic. Plant Physiol 141:288–298CrossRefGoogle Scholar
  50. Li J-Y, Fu Y-L, Pike SM, Bao J, Tian W, Zhang Y, Chen C-Z et al (2010) The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell 22:1633–1646CrossRefGoogle Scholar
  51. Liu T, Liu S, Guan H, Ma L, Chen Z, Gu H, Qu L-J (2009) Transcriptional profiling of Arabidopsis seedlings in response to heavy metal lead (Pb). Environ Exp Bot 67:377–386CrossRefGoogle Scholar
  52. Ludewig U, Fromme WB (2002) Genes and proteins for solute transport and sensing. In: Somerville CR, Meyerowitz EM (eds) The arabidopsis book. American Society of Plant Biologists, Rockville, http://www.aspb.org/publications/arabidopsis/ - this publication is only available as an on-line textGoogle Scholar
  53. Ludwig-Müller J (2007) Indole-3-butyric acid synthesis in ecotypes and mutants of Arabidopsis thaliana under different growth conditions. J Plant Physiol 164:47–59CrossRefGoogle Scholar
  54. Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37CrossRefGoogle Scholar
  55. Magidin M, Pittman JK, Hirschi KD, Bartel B (2003) ILR2, a novel gene regulating IAA conjugate sensitivity and metal transport in Arabidopsis thaliana. Plant J 35:523–534CrossRefGoogle Scholar
  56. Maksymiec W, Krupa Z (2002) Jasmonic acid and heavy metals in Arabidopsis plants – a similar physiological response to both stressors? J Plant Physiol 159:509–515CrossRefGoogle Scholar
  57. Maksymiec W, Krupa Z (2006) The effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ Exp Bot 57:187–194CrossRefGoogle Scholar
  58. Maksymiec W, Wianowska D, Dawidowicz AL, Radkiewiczb S et al (2005) The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. J Plant Physiol 162:1338–1346CrossRefGoogle Scholar
  59. Maksymiec W, Wójcik M, Krupa Z (2007) Variation in oxidative stress and photochemical activity in Arabidopsis thaliana leaves subjected to cadmium and excess copper in the presence or absence of jasmonate and ascorbate. Chemosphere 66:421–427CrossRefGoogle Scholar
  60. McGrath SP, Lombi E, Gray CW, Caille N, Dunham SJ, Zhao FJ (2006) Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri. Environ Pollut 141:115–125CrossRefGoogle Scholar
  61. 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 151:715–731CrossRefGoogle Scholar
  62. Mira H, Martínez N, Peñarrubia L (2002) Expression of a vegetative-storage-protein gene from Arabidopsis is regulated by copper, senescence and ozone. Planta 214:939–946CrossRefGoogle Scholar
  63. Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, Tarkowska D et al (2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci U S A 103:16598–16603CrossRefGoogle Scholar
  64. 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 149:894–904CrossRefGoogle Scholar
  65. Murphy A, Taiz L (1995) Comparison of metallothionein gene expression and nonprotein thiols in ten Arabidopsis ecotypes. Correlation with copper tolerance. Plant Physiol 109:945–954CrossRefGoogle Scholar
  66. Ogawa S, Yoshidomi T, Yoshimura E (2011) Cadmium(II)-stimulated enzyme activation of Arabidopsis thaliana phytochelatin synthase 1. J Inorg Biochem 105:111–117CrossRefGoogle Scholar
  67. Pasternak T, Rudas V, Potters G, Jansen MAK (2005) Morphogenic effects of abiotic stress: reorientation of growth in Arabidopsis thaliana seedlings. Environ Exp Bot 53:299–314CrossRefGoogle Scholar
  68. 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 97:4956–4960CrossRefGoogle Scholar
  69. Peterson AG, Oliver DJ (2006) Leaf-targeted phytochelatin synthase in Arabidopsis thaliana. Plant Physiol Biochem 44:885–892CrossRefGoogle Scholar
  70. Połeć-Pawlak K, Ruzik R, Abramski K, Ciurzyńska M, Gawrońska H (2005) Cadmium speciation in Arabidopsis thaliana as a strategy to study metal accumulation system in plants. Anal Chim Acta 540:61–70CrossRefGoogle Scholar
  71. Pomponi M, Censi V, Di Girolamo V, De Paolis A, Sanità di Toppi L et al (2006) Overexpression of Arabidopsis phytochelatin synthase in tobacco plants enhances Cd2+ tolerance and accumulation but not translocation to the shoot. Planta 223:180–190CrossRefGoogle Scholar
  72. Prasad MNV (1995) Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 35:525–545CrossRefGoogle Scholar
  73. Przedpełska E, Wierzbicka M (2007) Arabidopsis arenosa (Brassicaceae) from a lead–zinc waste heap in southern Poland – a plant with high tolerance to heavy metals. Plant Soil 299:43–53CrossRefGoogle Scholar
  74. Remans T, Smeets K, Opdenakker K, Mathijsen D, Vangronsveld J, Cuypers A (2008) Normalization of real-time RT-PCR gene expression measurements in Arabidopsis thaliana exposed to increased metal concentrations. Planta 227:1343–1349CrossRefGoogle Scholar
  75. Remans T, Opdenakker K, Smeets K, Mathijsen D, Vangronsveld J, Cuypers A (2010) Metal-specific and NADPH oxidase dependent changes in lipoxygenase and NADPH oxidase gene expression in Arabidopsis thaliana exposed to cadmium or excess copper. Funct Plant Biol 37:532–544CrossRefGoogle Scholar
  76. Rogers EE, Eide DJ, Guerino ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci U S A 97:12356–12360CrossRefGoogle Scholar
  77. Roosens NHCJ, Willems G, Saumitou-Laprade P (2008) Using Arabidopsis to explore zinc tolerance and hyperaccumulation. Trends Plant Sci 13:208–215CrossRefGoogle Scholar
  78. Roth U, von Roepenack-Lahaye E, Clemens S (2006) Proteome changes in Arabidopsis thaliana roots upon exposure to Cd2+. J Exp Bot 57:4003–4013CrossRefGoogle Scholar
  79. Sanità di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130CrossRefGoogle Scholar
  80. Sanita di Toppi L, Gremigni P, Pawlik-Skowroska B, Prasad MNV, Cobbett CS (2003) Response to heavy metals in plants: a molecular approach. In: Toppi L, Pawlik-Skowroska B (eds) Abiotic stresses in plants. Kluwer Academic Publishers, Dordrecht, pp 133–156Google Scholar
  81. Sarret G, Saumitou-Laprade P, Bert V, Proux O, Hazemann J-L et al (2002) Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiol 130:1815–1826CrossRefGoogle Scholar
  82. Semane B, Dupae J, Cuypers A, Noben J-P, Tuomainen M, Tervahauta A et al (2010) Leaf proteome responses of Arabidopsis thaliana exposed to mild cadmium stress. J Plant Physiol 167:247–254CrossRefGoogle Scholar
  83. Sharma SS, Kumar V (2002) Responses of wild type and abscisic acid mutants of Arabidopsis thaliana to cadmium. J Plant Physiol 159:1323–1327CrossRefGoogle Scholar
  84. Singh N, Ma LQ (2007) Assessing plants for phytoremediation of arsenic-contaminated soils. In: Willey N (ed) Phytoremediation. Methods and reviews. Humana Press Inc., Totowa, pp 319–347CrossRefGoogle Scholar
  85. Skórzyńska-Polit E, Pawlikowska-Pawlęga B, Szczuka E, Drążkiewicz M, Krupa Z (2006) The activity and localization of lipoxygenases in Arabidopsis thaliana under cadmium and copper stresses. J Plant Growth Regul 48:29–39CrossRefGoogle Scholar
  86. Smeets K, Ruytinx J, Semane B, Van Belleghem F, Remans T, Van Sanden S et al (2008) Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot 63:1–8CrossRefGoogle Scholar
  87. Smeets K, Opdenakker K, Remans T, Van Sanden S, Van Belleghem F, Semane B et al (2009) Oxidative stress-related responses at transcriptional and enzymatic levels after exposure to Cd or Cu in a multipollution context. J Plant Physiol 166:1982–1992CrossRefGoogle Scholar
  88. Stacey MG, Patel A, McClain WE, Mathieu M, Remley M, Rogers EE, Gassmann W et al (2008) The Arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiol 146:589–601CrossRefGoogle Scholar
  89. Talke IN, Hanikenne M, Krämer 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 142:148–167CrossRefGoogle Scholar
  90. Tan-Kristanto A, Hoffmann A, Woods R, Batterham P, Cobbett C, Sinclair C (2003) Translational asymmetry as a sensitive indicator of cadmium stress in plants: a laboratory test with wild-type and mutant Arabidopsis thaliana. New Phytol 159(471):477Google Scholar
  91. Tehseen M, Cairns N, Sherson S, Cobbett CS (2010) Metallochaperone-like genes in Arabidopsis thaliana. Metallomics 2:556–564CrossRefGoogle Scholar
  92. Tennstedt P, Peisker D, Böttcher C, Trampczynska A, Clemens S (2009) Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiol 149:938–948CrossRefGoogle Scholar
  93. Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci U S A 97:4991–4996CrossRefGoogle Scholar
  94. Van Belleghem F, Cuypers A, Semane B, Smeets K, Vangronsveld J, d’Haen J, Valcke R (2007) Subcellular localization of cadmium in roots and leaves of Arabidopsis thaliana. New Phytol 173:495–508CrossRefGoogle Scholar
  95. van de Mortel JE, Almar Villanueva L, Schat H, Kwekkeboom J et al (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 142:1127–1147CrossRefGoogle Scholar
  96. 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 119:1047–1055CrossRefGoogle Scholar
  97. Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A et al (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794CrossRefGoogle Scholar
  98. Vanhoudt N, Vandenhove H, Smeets K, Remans T, Van Hees M et al (2008) Effects of uranium and phosphate concentrations on oxidative stress related responses induced in Arabidopsis thaliana. Plant Physiol Biochem 46:987–996CrossRefGoogle Scholar
  99. Vatamaniuk OK, Mari S, Yu-Ping L, Rea PA (1999) AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proc Natl Acad Sci U S A 96:7110–7115CrossRefGoogle Scholar
  100. Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:1–9CrossRefGoogle Scholar
  101. Watanabe A, Ito H, Chiba M, Ito A, Shimizu H, Fuji S, Nakamura S, Hattori H et al (2010) Isolation of novel types of Arabidopsis mutants with altered reactions to cadmium: cadmium-gradient agar plates are an effective screen for the heavy metal-related mutants. Planta 232:825–836CrossRefGoogle Scholar
  102. Waters BM, Chu H-H, DiDonato RJ, Roberts LA, Eisley RB, Lahner B, Salt DE, Walker EL (2006) Mutations in Arabidopsis Yellow Stripe-Like1 and Yellow Stripe-Like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141:1446–1458CrossRefGoogle Scholar
  103. Wienkoop S, Zoeller D, Ebert B, Simon-Rosin U, Fisahn J, Glinski M, Weckwerth W (2004) Cell-specific protein profiling in Arabidopsis thaliana trichomes: identification of trichome-located proteins involved in sulfur metabolism and detoxification. Phytochemistry 65:1641–1649CrossRefGoogle Scholar
  104. Wintz H, Fox T, Wu Y-Y, Feng V, Chen W, Chang H-S, Zhu T, Vulpe C (2003) Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J Biol Chem 278:47644–47653CrossRefGoogle Scholar
  105. Wojas S, Hennig 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 Pollut 157:2781–2789CrossRefGoogle Scholar
  106. Wójcik M, Tukiendorf A (2004) Phytochelatin synthesis and cadmium localization in wild type of Arabidopsis thaliana. J Plant Growth Regul 44:71–80CrossRefGoogle Scholar
  107. Wójcik M, Vangronsveld J, D’Haenc J, Tukiendorf A (2005a) Cadmium tolerance in Thlaspi caerulescens. II. Localization of cadmium in Thlaspi caerulescens. Environ Exp Bot 53:163–171Google Scholar
  108. Wójcik M, Vangronsveld J, Tukiendorf A (2005b) Cadmium tolerance in Thlaspi caerulescens I. Growth parameters, metal accumulation and phytochelatin synthesis in response to cadmium. Environ Exp Bot 53:151–161Google Scholar
  109. Wójcik M, Pawlikowska-Pawlęga B, Tukiendorf A (2009) Physiological and ultrastructural changes in Arabidopsis thaliana as affected by changed GSH level and Cu excess. Russ J Plant Physiol 56:820–829CrossRefGoogle Scholar
  110. Wong CKE, Cobbett CS (2009) HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181:71–78CrossRefGoogle Scholar
  111. 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 181:79–88CrossRefGoogle Scholar
  112. Zhang L, Ackley AR, Pilon-Smits EAH (2007) Variation in selenium tolerance and accumulation among 19 Arabidopsis thaliana accessions. J Plant Physiol 164:327–336CrossRefGoogle Scholar
  113. 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 57:3575–3582CrossRefGoogle Scholar
  114. Zimmermann M, Clarke O, Gulbis JM, Keizer DW, Jarvis RS, Cobbett CS, Hinds MG, Xiao Z, Wedd AG (2009) Metal binding affinities of Arabidopsis zinc and copper transporters: selectivities match the relative, but not the absolute, affinities of their amino-terminal domains. Biochemistry 48:11640–11654CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Dipartimento di Scienze dei Sistemi Colturali, Forestali e dell’AmbienteUniversità degli Studi della BasilicataPotenzaItaly
  2. 2.Centre for Environmental SciencesHasselt UniversityDiepenbeekBelgium

Personalised recommendations