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Reactive Oxygen Species and Signaling in Cadmium Toxicity

  • Luisa M. SandalioEmail author
  • María Rodríguez-Serrano
  • Luis A. del Río
  • María C. Romero-Puertas
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM)

Abstract

The toxicity of heavy metals in living organisms has become a major focus of research in recent decades as a result of the increased environmental pollution in industrial areas. Cadmium is one of the most dangerous heavy metals due to its high mobility in plants. This metal produces malfunctions in membranes, photosynthesis rate, and water-nutrient balance, and also causes oxidative damages. By contrast with the enormous number of publications on the tolerance and accumulation of cadmium in plants, there is a remarkable lack of knowledge on the molecular mechanisms and signaling events underlying plant responses to Cd toxicity, especially those involving reactive oxygen species (ROS). The dual role of ROS in heavy metal toxicity as both oxidative damage inducers and signaling molecules has been demonstrated in recent years and will be discussed in this chapter. The contribution of oxidative damage to Cd toxicity and the mechanisms involved in the cellular response to this metal, such as antioxidant regulation, protein defenses, and the role of NO and hormones, will also be analyzed.

Keywords

Reactive Oxygen Species Nitric Oxide Heavy Metal Salicylic Acid Reactive Oxygen Species Production 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by the Ministry of Education and Science, Spain (Grant BIO2005–03305) and Junta de Andalucía (project P06-CVI-01820).

References

  1. Aravind P, Narasimha M, Prasad V (2005) Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate-glutathione cycle and glutathione metabolism. Plant Physiol Biochem 43:107–116PubMedCrossRefGoogle Scholar
  2. Arisi AC, Mocquo B, Lagriffiould A, Mench M, Foyer CH, Jouanin L (2000). Responses to cadmium in leaves of transformed poplars overexpressing glutamylcysteine synthase. Physiol Plant 109:143–149CrossRefGoogle Scholar
  3. Arnaud N, Murgia I, Boucherez J, Briat JF, Cellier F, Gaymard F (2006) An iron-induced nitric oxide burst preceedes ubiquitin-dependent protein degradation for Arabidopsis AtFer1 ferritin gene expression. J Biol Chem 281:23579–23588PubMedCrossRefGoogle Scholar
  4. Azpilicueta CE, Benavides MP, Tomaro ML, Gallego S (2007) Mechanism of CATA3 induction by cadmium in sinflower leaves. Plant Physiol Biochem 45:589–595PubMedCrossRefGoogle Scholar
  5. Bartha B, Kolbert Z, Erdei L (2005) Nitric oxide production induced by heavy metals in Brassica juncea L. Czern. and Pisum sativum L. Acta Biol Szeg 49:9–12Google Scholar
  6. Békésiová B, Hraška S, Libantová J, Moravcikova J, Matusšiková I (2008) Heavy-metal stress induced accumulation of chitinase isoforms in plants. Mol Biol Rep 35:579–588PubMedCrossRefGoogle Scholar
  7. Benavides MP, Gallego SM, Tomaro M (2005) Cadmium toxicity in plants. Brazil J Plant Physiol 17:21–34Google Scholar
  8. Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Ann Rev Plant Biol 59:21–39CrossRefGoogle Scholar
  9. Cho U, Seo N (2004) Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 168:113–120CrossRefGoogle Scholar
  10. Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719PubMedCrossRefGoogle Scholar
  11. Cobett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832CrossRefGoogle Scholar
  12. Collin V, Eymery F, Genty B, Rey P, Havaux M (2008) Vitamin E is essential for the tolerance of Arabidopsis thaliana to metal-induced oxidative stress. Plant Cell Environ 31:244–257PubMedGoogle Scholar
  13. Dana MM, Pintor-Toro JA, Cubero B (2006) Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol 142:722–730CrossRefGoogle Scholar
  14. Delledonne M (2005) NO news is good news for plants. Curr Opin Plant Biol 8:390–396PubMedCrossRefGoogle Scholar
  15. Devoto A, Turner JG (2005) Jasmonate-regulated Arabidopsis stress signaling network. Physiol Plant 123:161–172CrossRefGoogle Scholar
  16. Dixit V, Pandey V, Shymar R (2001). Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot 52:1101–1109PubMedCrossRefGoogle Scholar
  17. Djebali W, Gallusci P, Polge C, Boulila L, Galtier N, Raymond P, Chaibi W, Brouquisse R (2008) Modifications in endopeptidase and 20S proteasome expression and activities in cadmium treated tomato (Solanum lycopersicum L.) plants. Planta 227:625–639PubMedCrossRefGoogle Scholar
  18. Drazic G, Mihailovic N (2005) Modification of cadmium toxicity in soybean seedlings by salicylic acid. Plant Sci 168:511–517CrossRefGoogle Scholar
  19. Faller P, Kienzler K, Krieger-Liszkay A (2005) Mechanism of Cd2+ inhibits photoactivation of photosyntem II by competitive binding to the essential Ca2+ site. Biochim Biophys Acta 1706:158–164PubMedCrossRefGoogle Scholar
  20. 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 280:12168–12180PubMedCrossRefGoogle Scholar
  21. Fodor A, Szabó-Nagy A, Erdei l (1995) The effects of cadmium on the fluidity and H+-ATPase activity of plasma membrane from sunflower and wheat roots. J Plant Physiol 147:87–92CrossRefGoogle Scholar
  22. Freeman JL, Persana MW, Nieman K, Albretch C, Peer W, Pickering IJ, Salt DE (2004) Increased glutathione biosynthesis plays a role on nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176–2191PubMedCrossRefGoogle Scholar
  23. 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 137:1082–1091PubMedCrossRefGoogle Scholar
  24. Gallego SM, Benavides MO, Tomaro ML (1996) Effects of heavy-metal ion excess in sunflower leaves: evidences for involvement of oxidative stress. Plant Sci 121:151–159CrossRefGoogle Scholar
  25. Garnier L, Simon-Plas F, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 29:1956–1969PubMedCrossRefGoogle Scholar
  26. Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49PubMedCrossRefGoogle Scholar
  27. Guo B, Liang YC, Zhu YG, Zhao FJ (2007) Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress. Environ Pollut 147:743–749PubMedCrossRefGoogle Scholar
  28. Halliwell B, Gutteridge JMC (2007) Free Radicals in Biology and Medicine, 4th edition. Oxford University Press, LondonGoogle Scholar
  29. Herbette S, Taconnat L, Hugouvieux V, Piette L, Magniette ML, Cuine S, Auroy P, Richaud P, Forestier C, Bourguignon J, Renou JP, Vavasseur A, Leonhardt N (2006) Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88:1751–1765PubMedCrossRefGoogle Scholar
  30. Hernández LE, Cooke DT (1997) Modification of the root plasma membrane lipid composition of cadmium-treated Pisum sativum. J Exp Bot 48:1375–1381CrossRefGoogle Scholar
  31. Hernández LE, Lozano-Todróguez E, Gárate A, Carpena-Ruíz R (1998) Influence of cadmium on the uptake, tissue accumulation and subcellular distribution of manganese in pea seedlings. Plant Sci 132:139–151CrossRefGoogle Scholar
  32. Horemans N, Raeymaekers T, Van Beek K, Nowocin A, Blust R, Broos K, Cuypers A, Vangronsveld J, Guisez Y (2007). Dehydroascorbate uptake is impaired in the early response of Arabidopsis plant cell cultures to cadmium. J Exp Bot 16:4307–4317CrossRefGoogle Scholar
  33. Howarth JR, Domínguez-Solís JR, Gutiérrez-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 51:589–598PubMedCrossRefGoogle Scholar
  34. Howden R, Goldsbrough PB, Andersen CS, Cobbett CS (1995) Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol 107:1059–1066PubMedCrossRefGoogle Scholar
  35. Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238CrossRefGoogle Scholar
  36. Illéš P, Schlicht M, Pavlovkin J, Lichtscheidl I, Baluška F, Ovecka M (2006) Aluminium toxicity in plants: internalization of aluminium into cells of the transition zone in Arabidopsis roots apices related to changes in plasma membrane potential, endosomal behavior, and nitric oxide production. J Exp Bot 57:4201–4213PubMedCrossRefGoogle Scholar
  37. Jasinski M, Sudre D, Schansker G, Schellenberg M, Constant S, Martinoia E, Bovet L (2008) AtOSA1, a member of the Abc1-like family, as a new factor in cadmium and oxidative stress response. Plant Physiol 147:719–731PubMedCrossRefGoogle Scholar
  38. 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 50:207–218PubMedCrossRefGoogle Scholar
  39. Kopyra M, Gwóždž EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41:1011–1017CrossRefGoogle Scholar
  40. Kopyra M, Stachín-Wilk M, Gwóždž EA (2006) Effect of exogenous nitric oxide on the antioxidant capacity of cadmium-treated soybean cell suspension. Acta Physiol Plant 28:525–536CrossRefGoogle Scholar
  41. Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330CrossRefGoogle Scholar
  42. Lemaire S, Keryer E, Stein M, Schepens I, Issakidis-Bourguet E, Gérard-Hirme C, Miginiac-Maslow M, Jacquot JP (1999). Heavy-metal regulation of thioredoxin gene expression in Chlamydomonas reinhardti. Plant Physiol 120:773–778PubMedCrossRefGoogle Scholar
  43. Lindermayr C, Saalbach G, Bahnweg G, Durner J (2006) Differential inhibition of Arabidopsis methionine adenosyltransferases by protein S-nitrosylation. J Biol Chem 281:4285–4291PubMedCrossRefGoogle Scholar
  44. León AM, Palma JM, Corpas FJ, Gomez M, Romero-Puertas MC, Chatterjee D, Mateos RM, del Río LA, Sandalio LM (2002) Antioxidative enzymes in cultivars of pepper plants with different sensitivity to cadmium. Plant Physiol Biochem 40:813–820CrossRefGoogle Scholar
  45. Loake G, Grant M (2007) Salicylic acid in plant defense - the players and protagonists. Curr Opin Plant Biol 10:466–472PubMedCrossRefGoogle Scholar
  46. López-Martín MC, Becana M, Romero LC, Gotor C (2008) Knocking out cytosolic cysteine synthesis compromises the antioxidant capacity of the cytosol to maintain discrete concentrations of hydrogen peroxide in Arabidopsis. Plant Physiol 147:562–572PubMedCrossRefGoogle Scholar
  47. Ma CH, Haslbeck M, Babujee L, Jahn O, Reumann S (2006) Identification and characterization of a stress-inducible and a constitutive small heat-shock protein targeted to the matrix of plant peroxisomes. Plant Physiol 141:47–60PubMedCrossRefGoogle Scholar
  48. McCarthy I, Romero-Puertas MC, Palma JM, Sandalio LM, Corpas FJ, Gómez M, del Río LA (2001) Cadmium induces senescence symptoms in leaf peroxisomes of pea plants. Plant Cell Environ 24:1065–1073CrossRefGoogle Scholar
  49. Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003). Salicylic acid alleviates the cadmium toxicity in barley seedling. Plant Physiol 132:272–281PubMedCrossRefGoogle Scholar
  50. Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum. J Exp Bot 56:167–178PubMedGoogle Scholar
  51. Minglin L, Yuxiu Z, Tuanyao C (2005) Identification of genes up-regulated in response to Cd exposure in Brassica juncea L. Gene 363:151–158PubMedCrossRefGoogle Scholar
  52. Mithöfer A, Schulze B, Boland W (2004) Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett 566:1–5PubMedCrossRefGoogle Scholar
  53. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedCrossRefGoogle Scholar
  54. Mittler G, Mittler R (2006) Could heat shock transcription factor function as hydrogen peroxide sensor in plants? Ann Bot 98:279–288PubMedCrossRefGoogle Scholar
  55. Montillet JL, Cacas JL, Garnier L, Montané MH, Douki T, Bessoule JJ, Polkowska-Kowalczyk L, Maciejewska U, Agnel JP, Vial A, Triantaphylidès V (2004) The usptream oxylipin profile of Arabidopsis thaliana: a tool to scan for oxidative stresses. Plant J 40:439–451PubMedCrossRefGoogle Scholar
  56. Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian JC, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141:1138–1148PubMedCrossRefGoogle Scholar
  57. Obregón P, Marín R, Sanz A, Castresana C (2001) Activation of defense-related genes during senescence: a correlation between gen expression and cellular damage. Plant Mol Biol 46:67–77PubMedCrossRefGoogle Scholar
  58. Olmos E, Martinez-Solano JR, Piqueras A, Hellin E (2003) Early steps in the oxidative burst induced by cadmium in cultured tobacco cells (BY-2 line). J Exp Bot 54:291–301PubMedCrossRefGoogle Scholar
  59. Ortega-Villasante C, Rellán-Álvarez ZZ, Del Campo FF, Carpena-Ruiz RO, Hernández LE (2005) Cellular damage induced by cadmium and mercury in Medicago sativa. J Exp Bot 56:2239–2251PubMedCrossRefGoogle Scholar
  60. Ouariti O, Boussama N, Zarrouk M, Cherif A, Ghorbal MH (1997) Cadmium and copper-induced changes in tomato membrane lipids. Phytochem 45:1343–1350CrossRefGoogle Scholar
  61. Ouelhadj A, Kuschk P, Humbeck K (2006) Heavy metal stress and leaf senescence induce the barley gene HvC2d1 encoding a calcium-dependent novel C2 domain-like protein. New Phytol 170:261–273PubMedCrossRefGoogle Scholar
  62. Paradiso A, Berardino R, de Pinto MC, Sanitá di Toppi L, Srotelli MM, Tommasi F, de Gara L (2008) Increase in the ascorbate-glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol 49:362–374PubMedCrossRefGoogle Scholar
  63. Pena LB, Pasquini LA, Tomaro ML, Gallego SM (2006) Proteolytic system in sunflower (Helianthus annuus L.) leaves under cadmium stress. Plant Sci 171:531–537CrossRefGoogle Scholar
  64. Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32:539–548PubMedCrossRefGoogle Scholar
  65. Poschenrieder C, Gunsé B, Barceló J (1989) Influence of cadmium on water relations, stomatal resistance, and abscisic acid content in expanding bean leaves. Plant Physiol 90:1365–1371PubMedCrossRefGoogle Scholar
  66. del Río LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006). Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging and role in cell signaling. Plant Physiol 141:330–335PubMedCrossRefGoogle Scholar
  67. Rivetta A, Negrini N, Cocucci M (1997) Involvement of Ca2+-calmodulin in Cd2+ toxicity during the early phases of radish (Raphanus sativus L.) seed germination. Plant Cell Environ 20:600–608CrossRefGoogle Scholar
  68. Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, del Río LA, Sandalio, LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544PubMedCrossRefGoogle Scholar
  69. 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 150:229–243PubMedCrossRefGoogle Scholar
  70. Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci USA 97:12356–12360PubMedCrossRefGoogle Scholar
  71. Romero-Puertas MC, McCarthy I, Sandalio LM, Palma JM, Corpas FJ, Gómez M, del Río LA. (1999) Cadmium toxicity and oxidative metabolism of pea leaf peroxisomes. Free Rad Res 31:S25–S32CrossRefGoogle Scholar
  72. Romero-Puertas MC, Palma JM, Gómez M, del Río LA, Sandalio LM (2002) Cadmium causes the modification of proteins in pea plants. Plant Cell Environ 25:677–686CrossRefGoogle Scholar
  73. Romero-Puertas MC, Rodríguez-Serrano M, Corpas FJ, Gómez M, del Río LA, Sandalio LM (2004) Cadmium-induced subcellular accumulation of O2·− and H2O2 in pea leaves. Plant Cell Environ 27:1122–1134CrossRefGoogle Scholar
  74. Romero-Puertas MC, Corpas FJ, Rodriguez-Serrano M, Gomez M, del Río LA, Sandalio LM (2007a) Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. J Plant Physiol 164:1346–1357CrossRefGoogle Scholar
  75. Romero-Puertas MC, Laxa M, Mattè A, Zanninotto F, Finkemeier I, Jones AME, Perazzolli M, Vandelle E, Dietz KJ, Delledonne M (2007b) S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19:4120–4130CrossRefGoogle Scholar
  76. Romero-Puertas MC, Campostrini N, Matte A, Righetti PG, Perazzolli M, Zolla L, Roepstorff P, Delledonne M (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics 8:1459–1469PubMedCrossRefGoogle Scholar
  77. Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126PubMedGoogle Scholar
  78. Sanitá di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130CrossRefGoogle Scholar
  79. Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V, Jourdain A, Bastien O,Fievet J, Vailhen D, Amekraz B, Moulin C, Ezan C, Garin J, Bourguignon J (2006) The early response of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analysis. Proteomics 6:2180–2198PubMedCrossRefGoogle Scholar
  80. Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metals-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365PubMedCrossRefGoogle Scholar
  81. Schützendübel A, Schwanz P, Terchmann T, Gross K, Langenfeld-Heyger R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in scots pine roots. Plant Physiol 127:887–898PubMedCrossRefGoogle Scholar
  82. Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726PubMedCrossRefGoogle Scholar
  83. Shi QH, Zhu ZJ (2008) Effects of exogenous salicylic acid on manganese toxicity, element contents and antioxidative system in cucumber. Environ Exp Bot 63:1–3CrossRefGoogle Scholar
  84. Singh HP, Batish DR, Kaur G, Arora K, Kohli RK (2008) Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot 63:158–167CrossRefGoogle Scholar
  85. Skorzynska-Polit E, Krupa Z (2006) Lipid peroxidation in cadmium-treated Phaseolus coccineus plants. Arch Environ Contam Toxicol 50:482–487PubMedCrossRefGoogle Scholar
  86. Smeets K, Cuypers A, Lambrechts A, Semane B, Hoet P, Van Laere A, Vangronsveld J (2005). Induction of oxidative stress and antioxidative mechanisms in Phaseolus vulgaris after Cd application. Plant Physiol Biochem 43:437–444PubMedCrossRefGoogle Scholar
  87. Smeets K, Ruytinx J, Semane B, Van Belleghem F, Remans T, Van Saden S, Vanginsveld J, Cuypers A (2008) Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot 63:1–8CrossRefGoogle Scholar
  88. 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 135:1027–1039PubMedCrossRefGoogle Scholar
  89. Sunkar R, Kapoot A, Zhu J-K (2006). Posttranscripctional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by down-regulation of miT398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065PubMedCrossRefGoogle Scholar
  90. Suzuki N, Yamaguchi Y, Koizumi N, Sano H (2002) Functional characterization of a heavy metal binding protein CdI19 from Arabidopsis. Plant J 32:165–173PubMedCrossRefGoogle Scholar
  91. Suzuki N (2005) Alleviation by calcium of cadmium-induced root growth inhibition in Arabidopsis seedlings. Plant Biotechnol 22:19–25CrossRefGoogle Scholar
  92. Tian QY, Sun DH, Zhao MG, Zhang WH (2007) Inhibition of nitric oxide synthase (NOS) underlies aluminium-induced inhibition of root elongation in Hibiscus moscheutos. New Phytol 174:322–331PubMedCrossRefGoogle Scholar
  93. Tsyganov VE, Belimov AA, Borisov AY, Safronova VI, Georgi M, Dietz KJ, Tikhonovich IA (2007) A chemically induced new pea (Pisum sativum) mutant SGECdt with increased tolerance to, and accumulation of, cadmium. Annal Bot 99:227–237CrossRefGoogle Scholar
  94. Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206CrossRefGoogle Scholar
  95. Van Breusegem F, Bailey-Serres J, Mittler R (2008) Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 147:978–984PubMedCrossRefGoogle Scholar
  96. Van de Mortel JE, Schat H, Moerland PD, Ver Loren van Themaat E, van der Ent S, Blankestijn H, Ghandilyan A, Tsiatsiani S, Aarts MG (2008) Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 31:301–324PubMedCrossRefGoogle Scholar
  97. Vitória AP, Lea PJ, Azevedo RA (2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochem 57:701–710CrossRefGoogle Scholar
  98. Wang Y, Fang J, Leonard SS, Rao KM (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 36:1434–1443PubMedCrossRefGoogle Scholar
  99. Wang JW, Wu JY (2005) Nitric oxide is involved in methyl jasmonate-induced defense responses and secondary metabolism activities of Taxus xells. Plant Cell Physiol 46:923–930PubMedCrossRefGoogle Scholar
  100. Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923PubMedCrossRefGoogle Scholar
  101. Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd(2+)-hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 29:950–963PubMedCrossRefGoogle Scholar
  102. Wilson ID, Neill SJ, Hancock JT (2007) Nitric oxide synthesis and signaling in plants. Plant Cell Environ 31:622–631PubMedCrossRefGoogle Scholar
  103. Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550PubMedCrossRefGoogle Scholar
  104. Yu CC, Hung KT, Kao CH (2005) Nitricoxide reduces Cu toxicity and Cu-induced NH4+ accumulation in rice leaves. J Plant Physiol 162:1319–1330PubMedCrossRefGoogle Scholar
  105. Zhang H, Jiang Y, He Z, Ma M (2005) Cadmium accumulation and oxidative burst in garlic (Allium sativum). J Plant Physiol 162:977–984PubMedCrossRefGoogle Scholar
  106. Zhang LP, Mehta SK, Liu ZP, Yang ZM (2008) Copper-induced proline synthesis is associated with nitric oxide generation in Chlamydomonas reinhardtii. Plant Cell Physiol. 49:411–419PubMedCrossRefGoogle Scholar
  107. Zhao Z, Cai Y, Zhu Y, Kneer R (2005) Cadmium-induced oxidative stress and protection by l-galactono-1,4-lactone in winter wheat (Triticum aestivum L.). J Plant Nutr Soil Sci 168:1–5CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  • Luisa M. Sandalio
    • 1
    Email author
  • María Rodríguez-Serrano
    • 1
  • Luis A. del Río
    • 1
  • María C. Romero-Puertas
    • 1
  1. 1.Departamento de Bioquímica, Biología Celular y Molecular de PlantasEstación Experimental del Zaidín (CSIC)GranadaSpain

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