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Insights into Cadmium Toxicity: Reactive Oxygen and Nitrogen Species Function

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Metal Toxicity in Plants: Perception, Signaling and Remediation

Abstract

Cadmium (Cd) is a heavy metal that enters the environment mainly due to phosphate fertilizers and processes derived from industry and mining. This metal is a toxic element and the main problem of its accumulation is the rapid transference into the food chain through plants that take up the metal by their roots from where it can be loaded into the xylem for its transport into the leaves and fruits. Cd inhibits plant growth producing alterations in the photosynthesis rate, water use efficiency and the uptake and distribution of micro- and macro-nutrients. Additionally, Cd disturbs the plant antioxidant system and induces the production of reactive oxygen species (ROS) leading to an oxidative stress. Because Cd does not participate in Fenton-type reactions, the mechanisms by which Cd induces ROS production are not well understood. Recently, nitric oxide (NO), a well-known messenger in plants, has been involved in the plant Cd response although its function and sources are still largely unknown. In this chapter, we will discuss the effect of Cd on plants, the responses of the plant to the metal showing the proteomic and transcriptomic analysis that have been done in recent years and the role of ROS and NO in this response.

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References

  • Aina R, Labra M, Fumagalli P, Vannini C, Marsoni M, Cucchi U, Bracale M, Sgorbati S, Citterio S (2007) Thiol-peptide level and proteomic changes in response to cadmium toxicity in Oryza sativa L. roots. Environ Exp Bot 59:381–392

    CAS  Google Scholar 

  • Alloway BJ, Steinnes E (1999) Antropogenic additions of cadmium to soils. In: Cadmium in soils and plants. Kluwer, Dordrecht

    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

    PubMed  CAS  Google Scholar 

  • Alvarez S, Berla BM, Sheffield J, Cahoon RE, Jez JM, Hicks LM (2009) Comprehensive analysis of the Brassica juncea root proteome in response to cadmium exposure by complementary proteomic approaches. Proteomics 9:2419–2431

    PubMed  CAS  Google Scholar 

  • Aravind P, Prasad MN (2005) Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate-glutathione cycle and glutathione metabolism. Plant Physiol Biochem 43:107–116

    PubMed  CAS  Google Scholar 

  • Aravind P, Prasad MNV, Malec P, Waloszek A, Strzalka K (2009) Zinc protects Ceratophyllum demersum L. (free-floating hydrophyte) against reactive oxygen species induced by cadmium. J Trace Elem Med Biol 23:50–60

    PubMed  CAS  Google Scholar 

  • Azcón R, Peralvarez MC, Roldan A, Barea JM (2010) Arbuscular mycorrhizal fungi, Bacillus cereus, and Candida parapsilosis from a multicontaminated soil alleviate metal toxicity in plants. Microb Ecol 59:668–677

    PubMed  Google Scholar 

  • Azevedo H, Pinto C, Santos C (2005) Cd effects in sunflower: nutritional imbalances in plants and calluses. J Plant Nutr 28:2221–2231

    CAS  Google Scholar 

  • Azpilicueta CE, Benavides MP, Tomaro ML, Gallego SM (2007) Mechanism of CATA3 induction by cadmium in sunflower leaves. Plant Physiol Biochem 45:589–595

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Bartha B, Kolbert Z, Erdei L (2005) Nitric oxide production induced by heavy metals in Brassica juncea L.Cern. and Pisum sativum L. In: Proceedings of the 8th Hungarian Congress of Plant Physiology and the 6th Hungarian Conference of Photosyntesis. Hungary

    Google Scholar 

  • Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol 129:1642–50

    PubMed  CAS  Google Scholar 

  • Benavides MP, Gallego MS, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34

    CAS  Google Scholar 

  • Berezin I, Mizrachy-Dagry T, Brook E, Mizrahi K, Elazar M, Zhuo S, Saul-Tcherkas V, Shaul O (2008) Overexpression of AtMHX in tobacco causes increased sensitivity to Mg2+, Zn2+, and Cd2+ ions, induction of V-ATPase expression, and a reduction in plant size. Plant Cell Rep 27:939–949

    PubMed  CAS  Google Scholar 

  • Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39

    PubMed  CAS  Google Scholar 

  • Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, Pugin A, Wendehenne D (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 149:1302–1315

    PubMed  CAS  Google Scholar 

  • Bi Y, Chen W, Zhang W, Zhou Q, Yun L, Xing D (2009) Production of reactive oxygen species, impairment of photosynthetic function and dynamic changes in mitochondria are early events in cadmium-induced cell death in Arabidopsis thaliana. Biol Cell 101:629–643

    PubMed  CAS  Google Scholar 

  • Blum W (1997) Cadmium uptakeby higher plants. In: Proceedings of extendedabstracts from the Fourth International Conference on the Biogeochemistry of Trace Elements. University of California, Berkrley, USA, pp 109–110

    Google Scholar 

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

    CAS  Google Scholar 

  • Bovet L, Feller U, Martinoia E (2005) Possible involvement of plant ABC transporters in cadmium detoxification: a cDNA sub-microarray approach. Environ Int 31:263–267

    PubMed  CAS  Google Scholar 

  • Cataldo DA, Garland TR, Wildung RE (1983) Cadmium uptake kinetics in intact soybean plants. Plant Physiol 73:844–848

    PubMed  CAS  Google Scholar 

  • Chaoui A, Mazhoudi S, Ghorbal M (1997) Cadmiun and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean. Plant Sci 127:139–147

    CAS  Google Scholar 

  • 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 141:108–120

    PubMed  CAS  Google Scholar 

  • Chen F, Wang F, Wu F, Mao W, Zhang G, Zhou M (2010) Modulation of exogenous glutathione in antioxidant defense system against Cd stress in the two barley genotypes differing in Cd tolerance. Plant Physiol Biochem 48:663–672

    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 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Courbot M, Diez L, Ruotolo R, Chalot M, Leroy P (2004) Cadmium-responsive thiols in the ectomycorrhizal fungus Paxillus involutus. Appl Environ Microbiol 70:7413–7417

    PubMed  CAS  Google Scholar 

  • Craciun AR, Courbot M, Bourgis F, Salis P, Saumitou-Laprade P, Verbruggen N (2006) Comparative cDNA-AFLP analysis of Cd-tolerant and -sensitive genotypes derived from crosses between the Cd hyperaccumulator Arabidopsis halleri and Arabidopsis lyrata ssp. petraea. J Exp Bot 57:2967–2983

    PubMed  Google Scholar 

  • Cuypers A, Smeets K, Ruytinx J, Opdenakker K, Keunen E, Remans T, Horemans N, Vanhoudt N, Van Sanden S, Van Belleghem F, Guisez Y, Colpaert J, Vangronsveld J (2011) The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol 168:309–316

    PubMed  CAS  Google Scholar 

  • Das P, Samantaray S, Rou G (1997) Studies of cadmium toxicity in plants: a review. Environ Poll 98:29–36

    CAS  Google Scholar 

  • De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, di Toppi LS, Lo Schiavo F (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217–228

    PubMed  Google Scholar 

  • del Río LA (2011) Peroxisomes as a cellular source of reactive nitrogen species signal molecules. Arch Biochem Biophys 506:1–11

    PubMed  Google Scholar 

  • del Río LA, Puppo A (2009) Reactive oxygen species in plant signaling. Springer, Germany

    Google Scholar 

  • del Río LA, Corpas FJ, Barroso JB (2004) Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 65:783–792

    PubMed  Google Scholar 

  • 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 141:330–335

    PubMed  Google Scholar 

  • Delledonne M (2005) NO news is good news for plants. Curr Opin Plant Biol 8:390–396

    PubMed  CAS  Google Scholar 

  • Dietz KJ, Jacob S, Oelze ML, Laxa M, Tognetti V, de Miranda SM, Baier M, Finkemeier I (2006) The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 57:1697–1709

    PubMed  CAS  Google Scholar 

  • Ding Y, Chen Z, Zhu C (2011) Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot. doi:DOI:10.1093/jxb/err046

  • Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot 52:1101–1109

    PubMed  CAS  Google Scholar 

  • Durand TC, Sergeant K, Planchon S, Carpin S, Label P, Morabito D, Hausman JF, Renaut J (2010) Acute metal stress in Populus tremula x P. alba (717-1B4 genotype): leaf and cambial proteome changes induced by Cd 2+. Proteomics 10:349–368

    PubMed  CAS  Google Scholar 

  • Fagioni M, Zolla L (2009) Does the different proteomic profile found in apical and basal leaves of spinach reveal a strategy of this plant toward cadmium pollution response? J Proteome Res 8:2519–2529

    PubMed  CAS  Google Scholar 

  • Faller P, Kienzler K, Krieger-Liszkay A (2005) Mechanism of Cd2+ inhibits photoactivation of photosystem II by competitive binding to the essential Ca2+ site. Biochim Biophys Acta 1706:158–164

    PubMed  CAS  Google Scholar 

  • Farinati S, Dalcorso G, Panigati M, Furini A (2011) Interaction between selected bacterial strains and Arabidopsis halleri modulates shoot proteome and cadmium and zinc accumulation. J Exp Bot. doi:10.1093/jxb/err015

  • Fatima RA, Ahmad M (2005) Certain antioxidant enzymes of Allium cepa as biomarkers for the detection of toxic heavy metals in wastewater. Sci Total Environ 346:256–273

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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 14:787–792

    Google Scholar 

  • Foresi N, Correa-Aragunde N, Parisi G, Calóc G, Salernoc G, Lamattina L (2010) Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell 22:3816–3830

    PubMed  CAS  Google Scholar 

  • Fotjová M, Kovařik A (2000) Genotoxic effect of cadmium is associated with apoptotic changes in tobacco cells. Plant Cell Environ 23:531–537

    Google Scholar 

  • Fusco NM, 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 

  • 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 29:1956–1969

    PubMed  CAS  Google Scholar 

  • Godbold DL, Hutterman A (1985) Effect of zinc, cadmium and mercury on root elongation on Picea abies (Karst.) seedlings and the significance of these methals to forest die-back. Environ Pollut 38:375–381

    CAS  Google Scholar 

  • Gomes-Junior RA, Moldes CA, Delite FS, Pompeu GB, Gratao PL, Mazzafera P, Lea PJ, Azevedo RA (2006) Antioxidant metabolism of coffee cell suspension cultures in response to cadmium. Chemosphere 65:1330–1337

    PubMed  CAS  Google Scholar 

  • Gong JM, Lee DA, Schroeder JI (2003) Long-distance root-to-shoot transport of phytochelatins and cadmium in Arabidopsis. Proc Natl Acad Sci U S A 100:10118–10123

    PubMed  CAS  Google Scholar 

  • Gould K, Lamotte O, Klinguer A, Pugin A, Wendehenne D (2003) Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ 26:1851–1862

    CAS  Google Scholar 

  • Groppa MD, Rosales EP, Iannone MF, Benavides MP (2008) Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots. Phytochemistry 69:2609–2615

    PubMed  CAS  Google Scholar 

  • Gupta KJ, Kaiser WM (2010) Production and scavenging of nitric oxide by barley root mitochondria. Plant Cell Physiol 51:576–584

    PubMed  CAS  Google Scholar 

  • Gutteridge JM, Halliwell B (2000) Free radicals and antioxidants in the year 2000: a historical look to the future. Ann N Y Acad Sci 899:136–147

    PubMed  CAS  Google Scholar 

  • Haghiri F (1973) Plant uptake of cadmium as influenced by cation exchange capacity, organic matter, zinc and soil temperature. J Environ Qual 2:93–96

    CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Oxford University Press, New York

    Google Scholar 

  • Han Y, Zhang J, Chen X, Gao Z, Xuan W, Xu S, Ding X, Shen W (2008) Carbon monoxide alleviates cadmium-induced oxidative damage by modulating glutathione metabolism in the roots of Medicago sativa. New Phytol 177:155–166

    PubMed  CAS  Google Scholar 

  • Harada E, Kim JA, Meyer AJ, Hell R, Clemens S, Choi YE (2010) Expression profiling of tobacco leaf trichomes identifies genes for biotic and abiotic stresses. Plant Cell Physiol 51:1627–1637

    PubMed  CAS  Google Scholar 

  • 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 88:1751–1765

    PubMed  CAS  Google Scholar 

  • Hernandez LE, Carpena Ruiz RO, Garate A (1996) Alterations in the mineral nutrition of pea seedlings exposed to cadmium. J Plant Nutr 19:1581–1598

    CAS  Google Scholar 

  • Heyno E, Klose C, Krieger-Liszkay A (2008) Origin of cadmium-induced reactive oxygen species production: mitochondrial electron transfer versus plasma membrane NADPH oxidase. New Phytol 179:687–699

    PubMed  CAS  Google Scholar 

  • 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 58:4307–4317

    PubMed  CAS  Google Scholar 

  • Islam MM, Hoque MA, Okuma E, Jannat R, Banu MN, Jahan MS, Nakamura Y, Murata Y (2009) Proline and glycinebetaine confer cadmium tolerance on tobacco bright yellow-2 cells by increasing ascorbate-glutathione cycle enzyme activities. Biosci Biotechnol Biochem 73:2320–2323

    PubMed  CAS  Google Scholar 

  • Janouskova M, Pavlikova D, Vosatka M (2006) Potential contribution of arbuscular mycorrhiza to cadmium immobilisation in soil. Chemosphere 65:1959–1965

    PubMed  CAS  Google Scholar 

  • Jentschke G, Winter S, Godbold DL (1999) Ectomycorrhizas and cadmium toxicity in Norway spruce seedlings. Tree Physiol 19:23–30

    PubMed  CAS  Google Scholar 

  • Kieffer P, Dommes J, Hoffmann L, Hausman JF, Renaut J (2008) Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics 8:2514–2530

    PubMed  CAS  Google Scholar 

  • Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Simamoto K (2007) Calcium dependent protein kinases regulate the production or reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080

    PubMed  CAS  Google Scholar 

  • Kopyra M, Gwóźdź 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 41:1011–1017

    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 

  • Kovacik J, Gruz J, Hedbavny J, Klejdus B, Strnad M (2009) Cadmium and nickel uptake are differentially modulated by salicylic acid in Matricaria chamomilla plants. J Agric Food Chem 57:9848–9855

    PubMed  CAS  Google Scholar 

  • Kovalchuk I, Titov V, Hohn B, Kovalchuk O (2005) Transcriptome profiling reveals similarities and differences in plant responses to cadmium and lead. Mutat Res 570:149–161

    PubMed  CAS  Google Scholar 

  • Lane TW, Morel FM (2000) A biological function for cadmium in marine diatoms. Proc Natl Acad Sci U S A 97:4627–4631

    PubMed  CAS  Google Scholar 

  • Laspina NV, Groppa MD, Tomaro M, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330

    CAS  Google Scholar 

  • Lee K, Bae DW, Kim SH, Han HJ, Liu X, Park HC, Lim CO, Lee SY, Chung WS (2010) Comparative proteomic analysis of the short-term responses of rice roots and leaves to cadmium. J Plant Physiol 167:161–168

    PubMed  CAS  Google Scholar 

  • 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 40:813–820

    Google Scholar 

  • Lindermayr C, Saalbach G, Bahnweg G, Durner J (2006) Differential inhibition of Arabidopsis methionine adenosyltransferases by protein S-nitrosylation. J Biol Chem 281:4285–4291

    PubMed  CAS  Google Scholar 

  • Liu W, Zhou Q, Li P, Gao H, Han YP, Li XJ, Yang YS, Li Y (2009) DNA mismatch repair related gene expression as potential biomarkers to assess cadmium exposure in Arabidopsis seedlings. J Hazard Mater 167:1007–1013

    PubMed  CAS  Google Scholar 

  • Liu XM, Kim KE, Kim KC, Nguyen XC, Han HJ, Jung MS, Kim HS, Kim SH, Park HC, Yun DJ, Chung WS (2010) Cadmium activates Arabidopsis MPK3 and MPK6 via accumulation of reactive oxygen species. Phytochemistry 71:614–618

    PubMed  CAS  Google Scholar 

  • López-Huertas E, Charlton WL, Johnson B, Graham IA, Baker A (2000) Stress induces peroxisome biogenesis genes. EMBO J 19:6770–6777

    PubMed  CAS  Google Scholar 

  • Louie M, Kondor N, DeWitt JG (2003) Gene expression in cadmium-tolerant Datura innoxia: detection and characterization of cDNAs induced in response to Cd2+. Plant Mol Biol 52:81–89

    PubMed  CAS  Google Scholar 

  • Maksymiec W, Wojcik 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 66:421–427

    PubMed  CAS  Google Scholar 

  • 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 24:1065–1073

    CAS  Google Scholar 

  • McLaughlin MJ, Singh BR (1999) Cadmium in soils and plants. In: Cadmium in soils and plants. Kluwer, Dordrecht

    Google Scholar 

  • Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281

    PubMed  CAS  Google Scholar 

  • Milone MT, Sgherri C, Clijsters H, Navarri-Izzo F (2003) Antioxidant responses of wheat treated with realistic concentration of cadmiun. Environ Exp Bot 50:265–276

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Morel FM, Malcolm EG (2005) The biogeochemistry of cadmium. Met Ions Biol Syst 43:195–219

    PubMed  CAS  Google Scholar 

  • Moreno JL, Hernandez T, Garcia C (1999) Effects of cadmium containing sewage sludge compost on dynamics of organic matter and microbial activity in an arid soils. Biol Fert Soils 28:230–237

    CAS  Google Scholar 

  • Muthukrishnan S, Liang G, Trick H, Gill B (2001) Pathogenesis-related proteins and their genes in cereals. Plant Cell Tiss Org 64:94–113

    Google Scholar 

  • Nawrot T, Plusquin M, Hogervorst J, Roels HA, Celis H, Thijs L, Vangronsveld J, Van Hecke E, Staessen JA (2006) Environmental exposure to cadmium and risk of cancer: a prospective population-based study. Lancet Oncol 7:119–126

    PubMed  CAS  Google Scholar 

  • Neill S, Bright J, Desikan R, Hancock J, Harrison J, Wilson I (2008) Nitric oxide evolution and perception. J Exp Bot 59:25–35

    PubMed  CAS  Google Scholar 

  • Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian JC, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141:1138–1148

    PubMed  CAS  Google Scholar 

  • Ogawa I, Nakanishi H, Mori S, Nishizawa N (2009) Time course analysis of gene regulation under cadmium stress in rice. Plant Soil 325:97–108

    CAS  Google Scholar 

  • 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 54:291–301

    PubMed  CAS  Google Scholar 

  • Ortega-Villasante C, Hernandez LE, Rellán-Alvarez R, Del Campo FF, Carpena-Ruiz RO (2007) Rapid alteration of cellular redox homeostasis upon exposure to cadmium and mercury in alfalfa seedlings. New Phytol 176:96–107

    PubMed  CAS  Google Scholar 

  • Ouariti O, Boussama N, Zarrouk M, Cherif A, Ghorbal MH (1997) Cadmium-and copper-induced changes in tomato membrane lipids. Phytochemistry 45:1343–1350

    PubMed  CAS  Google Scholar 

  • Pence NS, Larsen PB, Ebbs SD, Letham DL, 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

    PubMed  CAS  Google Scholar 

  • Pinto AP, Mota AM, de Varennes A, Pinto FC (2004) Influence of organic matter on the uptake of cadmium, zinc, copper and iron by sorghum plants. Sci Total Environ 326:239–247

    PubMed  CAS  Google Scholar 

  • Qian H, Li J, Sun L, Chen W, Sheng GD, Liu W, Fu Z (2009) Combined effect of copper and cadmium on Chlorella vulgaris growth and photosynthesis-related gene transcription. Aquat Toxicol 94:56–61

    PubMed  CAS  Google Scholar 

  • 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. Functional Plant Biol 37:532–544

    CAS  Google Scholar 

  • Ren D, Yang H, Zhang S (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem 277:559–565

    PubMed  CAS  Google Scholar 

  • Rodríguez-Celma J, Rellan-Alvarez R, Abadia A, Abadia J, Lopez-Millan AF (2010) Changes induced by two levels of cadmium toxicity in the 2-DE protein profile of tomato roots. J Proteomics 73:1694–1706

    PubMed  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gomez 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 29:1532–1544

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Sparkes I, Hawes C, del Río LA, Sandalio LM (2009b) Peroxisome dynamics in Arabidopsis plants under oxidative stress induced by cadmium. Free Radic Biol Med 47:1632–1639

    PubMed  Google Scholar 

  • Romero-Puertas MC, McCarthy I, Sandalio LM, Palma JM, Corpas FJ, Gomez M, del Río LA (1999) Cadmium toxicity and oxidative metabolism of pea leaf peroxisomes. Free Radic Res 31:25–31

    Google Scholar 

  • 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 25:677–686

    CAS  Google Scholar 

  • Romero-Puertas MC, Rodríguez-Serrano M, Corpas FJ, Gómez M, del Río LA, Sandalio LM (2004) Cadmium induced subcellular accumulation of O •–-2 and H2O2 in pea plants. Plant Cell Environ 27:1122–1134

    CAS  Google Scholar 

  • Romero-Puertas MC, Corpas FJ, Rodríguez-Serrano M, Gomez M, del Río LA, Sandalio LM (2007) Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. J Plant Physiol 164:1346–1357

    PubMed  CAS  Google Scholar 

  • 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 8:1459–1469

    PubMed  CAS  Google Scholar 

  • Romero-Puertas MC, Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmino DM, Gupta DK, Sandalio LM (2011) S-nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. Submitted

    Google Scholar 

  • Roth U, von Roepenack-Lahaye E, Clemens S (2006) Proteome changes in Arabidopsis thaliana roots upon exposure to Cd2+. J Exp Bot 57:4003–4013

    PubMed  CAS  Google Scholar 

  • 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 52:2115–2126

    PubMed  CAS  Google Scholar 

  • Sandalio LM, Rodríguez-Serrano M, del Río LA, Romero-Puertas MC (2009) Reactive oxygen species and signalling in cadmium toxicity. In: del Río LA, Puppo A (eds) Reactive oxygen species in plant signaling. Springer, Berlin/Heidelberg, pp 175–190

    Google Scholar 

  • Sanitá di Toppi L, Gabrielle R (1999) Response to Cadmiun in higher plants. Environ Exp Bot 41:105–130

    Google Scholar 

  • Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V, Jourdain A, Bastien O, Fievet JB, Vailhen D, Amekraz B, Moulin C, Ezan E, Garin J, Bourguignon J (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6:2180–2198

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol 127:887–898

    PubMed  Google Scholar 

  • Semane B, Dupae J, Cuypers A, Noben JP, Tuomainen M, Tervahauta A, Karenlampi S, Van Belleghem F, Smeets K, Vangronsveld J (2010) Leaf proteome responses of Arabidopsis thaliana exposed to mild cadmium stress. J Plant Physiol 167:247–254

    PubMed  CAS  Google Scholar 

  • 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 57:711–726

    PubMed  CAS  Google Scholar 

  • Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50

    PubMed  CAS  Google Scholar 

  • Shukla UC, Si J, Joshi PC, Kakkar P (2003) Effect of bioaccumulation of cadmium on biomass productivity, essential trace elements, chorophyl biosyntesis, and macromolecules of wheat seedlings. Biol Trace Elem Res 92:257–274

    PubMed  CAS  Google Scholar 

  • Smeets K, Opdenakker K, Remans T, Van Sanden S, Van Belleghem F, Semane B, Horemans N, Guisez Y, Vangronsveld J, Cuypers A (2009) Oxidative stress-related responses at transcriptional and enzymatic levels after exposure to Cd or Cu in a multipollution context. J Plant Physiol 166:1982–1992

    PubMed  CAS  Google Scholar 

  • Smiri M, Chaoui A, Rouhier N, Gelhaye E, Jacquot JP, El Ferjani E (2010) Cadmium affects the glutathione/glutaredoxin system in germinating pea seeds. Biol Trace Elem Res. doi:DOI:10.1007/s12011-010-8749-3

  • 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 

  • Souza VL, Almeida AA, Hora BT Jr, Gesteira AS, Cascardo JC (2008) Preliminary analysis of expressed sequences of genes in Genipa americana L. plant roots exposed to cadmium in nutrient solution. Genet Mol Res 7:1282–1288

    PubMed  CAS  Google Scholar 

  • Stohr C, Stremlau S (2006) Formation and possible roles of nitric oxide in plant roots. J Exp Bot 57:463–470

    PubMed  Google Scholar 

  • Stohr C, Strube F, Marx G, Ullrich WR, Rockel P (2001) A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta 212:835–841

    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 

  • Swoboda P, Gal S, Hohn B, Puchta H (1994) Intrachromosomal homologous recombination in whole plants. EMBO J. 13:484–489

    PubMed  CAS  Google Scholar 

  • Tamas L, Dudikova J, Durcekova K, Haluskova L, Huttova J, Mistrik I, Olle M (2008) Alterations of the gene expression, lipid peroxidation, proline and thiol content along the barley root exposed to cadmium. J Plant Physiol 165:1193–1203

    PubMed  CAS  Google Scholar 

  • 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 AtNRAMP genes. Proc Natl Acad Sci USA 97:4991–4996

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ueno D, Iwashita T, Zhao FJ, Ma JF (2008) Characterization of Cd translocation and identification of the Cd form in xylem sap of the Cd-hyperaccumulator Arabidopsis halleri. Plant Cell Physiol 49:540–548

    PubMed  CAS  Google Scholar 

  • Valko M, Morris H, Cronin MT (2005) Metals toxicity and oxidative stress. Curr Med Chem 12:1161–1208

    PubMed  CAS  Google Scholar 

  • van de Mortel JE, Schat H, Moerland PD, Loren V, 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 31:301–324

    PubMed  Google Scholar 

  • van Loon LC, van Strien EA (1999) The families of pathogenesisrelated proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant P 55:85–87

    Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372

    PubMed  CAS  Google Scholar 

  • Verkleij J, Schat H (1990) Mechanisms of methal tolerance in higher plants. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Boca Raton, pp 179–194

    Google Scholar 

  • Vitoria AP, Lea PJ, Azevedo RA (2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochemistry 57:701–710

    PubMed  CAS  Google Scholar 

  • Wagner GJ (1993) Accumulation of cadmium in crops plants and its consequences to human health. Adv Agron 51:173–212

    CAS  Google Scholar 

  • Wang JW, Wu JY (2005) Nitric oxide is involved in methyl jasmonate-induced defense responses and secondary metabolism activities of Taxus cells. Plant Cell Physiol 46:923–930

    PubMed  CAS  Google Scholar 

  • Watanabe A, Ito H, Chiba M, Ito A, Shimizu H, Fuji S, Nakamura S, Hattori H, Chino M, Satoh-Nagasawa N, Takahashi H, Sakurai K, Akagi H (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 232:825–836

    PubMed  CAS  Google Scholar 

  • 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 29:950–963

    PubMed  CAS  Google Scholar 

  • Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signalling in plants. Plant Cell Environ 31:622–631

    PubMed  CAS  Google Scholar 

  • Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550

    PubMed  CAS  Google Scholar 

  • Xiong J, An L, Lu H, Zhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765

    PubMed  CAS  Google Scholar 

  • Yakimova ET, Kapchina-Toteva VM, Laarhoven LJ, Harren FM, Woltering EJ (2006) Involvement of ethylene and lipid signalling in cadmium-induced programmed cell death in tomato suspension cells. Plant Physiol Biochem 44:581–589

    PubMed  CAS  Google Scholar 

  • Yamaguchi H, Fukuoka H, Arao T, Ohyama A, Nunome T, Miyatake K, Negoro S (2009) Gene expression analysis in cadmium-stressed roots of a low cadmium-accumulating solanaceous plant, Solanum torvum. J Exp Bot 61:423–437

    PubMed  Google Scholar 

  • Yang MG, Lin XY, Yang XE (1998) Impact of Cd on growth and nutrient accumulation of different plant species. Chin J Appl Ecol 19:89–94

    Google Scholar 

  • Yeh CM, Hsiao LJ, Huang HJ (2004) Cadmium activates a mitogen-activated protein kinase gene and MBP kinases in rice. Plant Cell Physiol 45:1306–1312

    PubMed  CAS  Google Scholar 

  • Zhang W, Chen W (2011) Role of salicylic acid in alleviating photochemical damage and autophagic cell death induction of cadmium stress in Arabidopsis thaliana. Photochem Photobiol Sci. doi:DOI:10.1039/C0PP00305K

  • Zhang ZC, Qiu BS (2007) Reactive oxygen species metabolism during the cadmium hyperaccumulation of a new hyperaccumulator Sedum alfredii (Crassulaceae). J Environ Sci (China) 19:1311–1317

    CAS  Google Scholar 

  • Zhang J, Hu M, Li JT, Guan JP, Yang B, Shu WS, Liao B (2009) A transcriptional profile of metallophyte Viola baoshanensis involved in general and species-specific cadmium-defense mechanisms. J Plant Physiol 166:862–870

    PubMed  CAS  Google Scholar 

  • Zhao FJ, Jiang RF, Dunham SJ, McGrath SP (2006) Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri. New Phytol 172:646–654

    PubMed  CAS  Google Scholar 

  • Zhao FJ, Ma JF, Meharg AA, McGrath SP (2008) Arsenic uptake and metabolism in plants. New Phytol 154:29–43

    Google Scholar 

  • Zhao CR, Ikka T, Sawaki Y, Kobayashi Y, Suzuki Y, Hibino T, Sato S, Sakurai N, Shibata D, Koyama H (2009) Comparative transcriptomic characterization of aluminum, sodium chloride, cadmium and copper rhizotoxicities in Arabidopsis thaliana. BMC Plant Biol 9:32

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported by Marie Curie Actions-European re-integration Grants (FP7-PEOPLE-2007-2-2-ERG; Project nº 208146), by ERDF-cofinanced grant BIO2008-04067 from MICINN and Junta de Andalucía (project P06-CVI-01820), Spain.

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  1. Departamento de Bioquímica, Biología Celular y Molecular de Plantas, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas (CSIC), Granada, Spain

    María C. Romero-Puertas, Ana P. Ortega-Galisteo, María Rodríguez-Serrano & Luisa M. Sandalio

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  1. María C. Romero-Puertas
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  2. Ana P. Ortega-Galisteo
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  3. María Rodríguez-Serrano
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  4. Luisa M. Sandalio
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Correspondence to María C. Romero-Puertas .

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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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Romero-Puertas, M.C., Ortega-Galisteo, A.P., Rodríguez-Serrano, M., Sandalio, L.M. (2012). Insights into Cadmium Toxicity: Reactive Oxygen and Nitrogen Species Function. 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_5

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