Skip to main content
SpringerLink
Log in

Metal/metalloid stress tolerance in plants: role of ascorbate, its redox couple, and associated enzymes

  • Review Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

The enhanced generation of reactive oxygen species (ROS) under metal/metalloid stress is most common in plants, and the elevated ROS must be successfully metabolized in order to maintain plant growth, development, and productivity. Ascorbate (AsA) is a highly abundant metabolite and a water-soluble antioxidant, which besides positively influencing various aspects in plants acts also as an enigmatic component of plant defense armory. As a significant component of the ascorbate-glutathione (AsA-GSH) pathway, it performs multiple vital functions in plants including growth and development by either directly or indirectly metabolizing ROS and its products. Enzymes such as monodehydroascorbate reductase (MDHAR, EC 1.6.5.4) and dehydroascorbate reductase (DHAR, EC 1.8.5.1) maintain the reduced form of AsA pool besides metabolically controlling the ratio of AsA with its oxidized form (dehydroascorbate, DHA). Ascorbate peroxidase (APX, EC 1.11.1.11) utilizes the reduced AsA pool as the specific electron donor during ROS metabolism. Thus, AsA, its redox couple (AsA/DHA), and related enzymes (MDHAR, DHAR, and APX) cumulatively form an AsA redox system to efficiently protect plants particularly against potential anomalies caused by ROS and its products. Here we present a critical assessment of the recent research reports available on metal/metalloid-accrued modulation of reduced AsA pool, AsA/DHA redox couple and AsA-related major enzymes, and the cumulative significance of these antioxidant system components in plant metal/metalloid stress tolerance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agius F, Gonzalez-Lamothe R, Caballero JL, Munoz-Blanco J, Botella MA, Valpuesta V (2003) Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase. Nat Biotechnol 21:177–181

    PubMed  CAS  Google Scholar 

  • Aksoy M, Dİnle BS (2012) Changes in physiological parameters and some antioxidant enzymes activities of soybean (Glycine max L. Merr.) leaves under cadmium and salt stress. J Stress Physiol Biochem 8:179–190

    Google Scholar 

  • Amako K, Chen GX, Asada K (1994) Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants. Plant Cell Physiol 35:497–504

    CAS  Google Scholar 

  • Anjum NA, Umar S, Ahmad A, Iqbal M (2008) Responses of components of antioxidant system in moongbean (Vigna radiata (L.) Wilczek) genotypes to cadmium stress. Commun Soil Sci Plant Anal 39:2469–2483

    CAS  Google Scholar 

  • Anjum NA, Umar S, Chan MT (eds) (2010) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Dordrecht

    Google Scholar 

  • Anjum NA, Umar S, Iqbal M, Khan NA (2011) Cadmium causes oxidative stress in mung mean by affecting the antioxidant enzyme system and ascorbate-glutathione cycle metabolism. Russ J Plant Physiol 58:92–99

    CAS  Google Scholar 

  • Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal M, Prasad MNV (2012a) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environ Exp Bot 75:307–324

    CAS  Google Scholar 

  • Anjum NA, Umar S, Ahmad A (2012b) Oxidative stress in plants: causes, consequences and tolerance. IK International Publishing House, New Delhi

    Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    PubMed  CAS  Google Scholar 

  • Aravind P, Prasad MNV (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 

  • Arrigoni O (1994) Ascorbate system in plant development. J Bioenerg Biomembr 26:407–419

    PubMed  CAS  Google Scholar 

  • Arrigoni O, De Tullio MC (2000) The role of ascorbic acid in cell metabolism: between gene-directed functions and unpredictable chemical reactions. J Plant Physiol 157:481–488

    CAS  Google Scholar 

  • Arrigoni O, De Tullio MC (2002) Ascorbic acid: much more than just an antioxidant. Biochim Biophys Acta 1569:1–9

    PubMed  CAS  Google Scholar 

  • Arrigoni O, Calabrese G, De Gara L, Bitonti MB, Liso R (1997) Correlation between changes in cell ascorbate and growth of Lupinus albus seedlings. J Plant Physiol 150:302–308

    CAS  Google Scholar 

  • Asada K (1992) Ascorbate peroxidase—a hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85:235–241

    CAS  Google Scholar 

  • Asada K (1993) Divergence of peroxide-scavenging peroxidases in organisms. In: Yagi K (ed) Active oxygens, lipid peroxides and antioxidants. CRC, Boca Raton, pp 289–298

    Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    PubMed  CAS  Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Bowler CB, Arntzen CB (eds) Photoinhibition. Elsevier, Amsterdam, pp 227–288

    Google Scholar 

  • Asard H, Horemans N, Caubergs RJ (1995) Involvement of ascorbic acid and a b-type cytochrome in plant plasma membrane redox reactions. Protoplasma 184:36–41

    CAS  Google Scholar 

  • Badejo AA, Fujikawa Y, Esaka M (2009) Gene expression of ascorbic acid biosynthesis related enzymes of the Smirnoff-Wheeler pathway in acerola (Malpighia glabra). J Plant Physiol 166:652–660

    PubMed  CAS  Google Scholar 

  • Balestrasse KB, Gardey L, Gallego SM, Tomaro ML (2001) Response of antioxidant defence system in soybean nodules and roots subjected to cadmium stress. Aust J Plant Physiol 28:497–504

    CAS  Google Scholar 

  • Barth C, De Tullio M, Conklin PL (2006) The role of ascorbic acid in the control of flowering time and the onset of senescence. J Exp Bot 57:1657–1665

    PubMed  CAS  Google Scholar 

  • Bartoli CG, Pastori GM, Foyer CH (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol 123:335–343

    PubMed  CAS  PubMed Central  Google Scholar 

  • Borracino G, Dipierro S, Arrigoni O (1986) Purification and properties of ascorbate free radical reductase from potato tubers. Planta 167:521–526

    Google Scholar 

  • Boveris A, Sies H, Martino EE, Docampo R, Turrens JF, Stoppani AO (1980) Deficient metabolic utilization of hydrogen peroxide in Trypanosoma cruzi. Biochem J 188:643–648

    PubMed  CAS  PubMed Central  Google Scholar 

  • Burkey KO, Eason G, Fiscus EL (2003) Factors that affect leaf extracellular ascorbic acid content and redox status. Physiol Plant 117:51–57

    CAS  Google Scholar 

  • Candan N, Tarhan L (2003) The correlation between antioxidant enzyme activities and lipid peroxidation levels in Mentha pulegium organs grown in Ca2+, Mg2+, Cu2+, Zn2+ and Mn2+ stress conditions. Plant Sci 165:769–776

    CAS  Google Scholar 

  • Carlos G, Pastori GM, Foyer CH (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol 123:335–343

    Google Scholar 

  • Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-Pinheiro M (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35:1011–1019

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chao YY, Hong CY, Kao CH (2010) The decline in ascorbic acid content is associated with cadmium toxicity of rice seedlings. Plant Physiol Biochem 48:374–381

    PubMed  CAS  Google Scholar 

  • Chen Z, Gallie DR (2006) Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol 142:775–787

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chen Z, Young TE, Ling J, Chang SC, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci U S A 100:3525–3530

    PubMed  CAS  PubMed Central  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 

  • Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877

    PubMed  CAS  Google Scholar 

  • Conklin PL, Barth C (2004) Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens, and the onset of senescence. Plant Cell Environ 27:959–970

    CAS  Google Scholar 

  • Conklin PL, Norris SR, Wheeler GL, Williams EH, Smirnoff N, Last RL (1999) Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. Proc Natl Acad Sci U S A 96:4198–203

    PubMed  CAS  PubMed Central  Google Scholar 

  • Córdoba F, Gonzales-Reyes JA (1994) Ascorbate and plant cell growth. J Bioenerg Biomembr 26:399–405

    PubMed  Google Scholar 

  • Córdoba-Pedregosa MC, Gonzalez-Reyes JA, Canadillas MS, Navas P, Cordoba F (1996) Role of apoplastic and cell-wall peroxidases on the stimulation of root elongation by ascorbate. Plant Physiol 112:1119–1125

    PubMed  PubMed Central  Google Scholar 

  • Córdoba-Pedregosa MC, Córdoba F, Villalba JM, José Antonio González-Reyes JA (2003) Zonal changes in ascorbate and hydrogen peroxide contents, peroxidase, and ascorbate-related enzyme activities in onion roots. Plant Physiol 131:697–706

    Google Scholar 

  • Cuypers A, Vangronsveld J, Clijsters H (2000) Biphasic effect of copper on the ascorbate-glutathione pathway in primary leaves of Phaseolus vulgaris seedlings during the early stages of metal assimilation. Physiol Plant 110:512–517

    CAS  Google Scholar 

  • Cuypers A, Remans T, Weyens N, Colpaert J, Vassilev A, Vangronsveld J (2013) Soil-plant relationships of heavy metals and metalloids. In: Alloway BJ (ed) Heavy metals in soils. Springer, Dordrecht, pp 161–193

    Google Scholar 

  • Dabrowska G, Kata A, Goc A, Szechynska-Hebda M, Skrzypek E (2007) Characteristics of the plant ascorbate peroxidase family. Acta Biol 49:7–17

    Google Scholar 

  • Dalton DA, Langeberg L, Robbins M (1992) Purification and characterization of monodehydroascorbate reductase from soybean root nodules. Arch Biochem Biophys 292:281–286

    PubMed  CAS  Google Scholar 

  • Davey MW, Van MM, Inze D, Sanmartin M, Kanellis A, Smirnoff N et al (2000) Plant L-ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. J Sci Food Agric 80:825–860

    CAS  Google Scholar 

  • De Gara L, Locato V, Dipierro S, de Pinto MC (2010) Redox homeostasis in plants. The challenge of living with endogenous oxygen production. Resp Physiol Neurobiol 173(Suppl):S13–S19

    Google Scholar 

  • De Leonardis S, De Lorenzo G, Borraccino G, Dipierro S (1995) A specific ascorbate free radical reductase isozyme participates in the regeneration of ascorbate for scavenging toxic oxygen species in potato tuber mitochondria. Plant Physiol 109:847–851

    PubMed  PubMed Central  Google Scholar 

  • De Leonardis S, Dipierro N, Dipierro S (2000) Purification and characterization of an ascorbate peroxidase from potato tuber mitochondria. Plant Physiol Biochem 38:773–779

    Google Scholar 

  • de Pinto MC, De Gara L (2004) Changes in the ascorbate metabolism of apoplastic and symplastic spaces are associated with cell differentiation. J Exp Bot 55:2559–2569

    PubMed  Google Scholar 

  • de Pinto MC, Francis D, De Gara L (1999) The redox state of the ascorbate-dehydroascorbate pair as a specific sensor of cell division in tobacco BY-2 cells. Protoplasma 209:90–97

    PubMed  Google Scholar 

  • de Pinto MC, Paradiso A, Leonetti P, De Gara L (2006) Hydrogen peroxide, nitric oxide and cytosolic ascorbate peroxidase at the crossroad between defence and cell death. Plant J 48:784–795

    PubMed  Google Scholar 

  • Debolt S, Melino V, Ford CM (2007) Ascorbate as a biosynthetic precursor in plants. Ann Bot 99:3–8

    PubMed  CAS  PubMed Central  Google Scholar 

  • Deleonardis S, Delorenzo G, Borraccino G, Dipierro S (1995) A specific ascorbate free radical reductase isozyme participates in the regeneration of ascorbate for scavenging toxic oxygen species in potato tuber mitochondria. Plant Physiol 109:847–851

    CAS  Google Scholar 

  • Dipierro N, Mondelli D, Paciolla C, Brunetti G, Dipierro S (2005) Changes in the ascorbate system in the response of pumpkin (Cucurbita pepo L.) roots to aluminium stress. J Plant Physiol 162:529–536

    PubMed  CAS  Google Scholar 

  • Diwan H, Ahmad A, Iqbal M (2008) Genotypic variation in the phytoremediation potential of Indian mustard for chromium. J Environ Manage 41:734–741

    Google Scholar 

  • Dong JG, Fernández-Maculet JC, Yang SF (1992) Purification and characterization of 1-aminocyclopropane-1-carboxylate oxidase from apple fruit. Proc Natl Acad Sci U S A 89:9789–9793

    PubMed  CAS  PubMed Central  Google Scholar 

  • Dowdle J, Ishikawa T, Gatzek S, Rolinski S, Smirnoff N (2007) Two genes in Arabidopsis thaliana encoding GDP-L-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. Plant J 52:673–689

    PubMed  CAS  Google Scholar 

  • Drew DP, Lunde C, Lahnstein J, Fincher GVB (2007) Heterologous expression of cDNAs encoding monodehydroascorbate reductases from the moss, Physcomitrella patens and characterization of the expressed enzymes. Planta 225:945–954

    PubMed  CAS  Google Scholar 

  • Eastmond PJ (2007) MONODEHYROASCORBATE REDUCTASE4 is required for seed storage oil hydrolysis and postgerminative growth in Arabidopsis. Plant Cell 19:1376–1387

    PubMed  CAS  PubMed Central  Google Scholar 

  • Eltayeb AE, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Shibahara T, Inanaga S, Tanaka K (2007) Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta 225:1255–1264

    PubMed  CAS  Google Scholar 

  • Fecht-Christoffers MM, Maier P, Horst WJ (2003) Apoplastic peroxidases and ascorbate are involved in manganese toxicity and tolerance of Vigna unguiculata. Physiol Plant 117:237–244

    CAS  Google Scholar 

  • Fiorani M, De Sanctis R, Scarlatti F, Vallorani L, De Bellis R, Serafini G, Bianchi M, Stocchi V (2000) Dehydroascorbic acid irreversibly inhibits hexokinase activity. Mol Cell Biochem 209:145–153

    PubMed  CAS  Google Scholar 

  • Fotopoulos V, Ziogas V, Tanou G, Molassiotis A (2010) Involvement of AsA/DHA and GSH/GSSG ratios in gene and protein expression and in the activation of defence mechanisms under abiotic stress conditions. In: Anjum NA, Umar S, Chan MT (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Dordrecht, pp 265–302

    Google Scholar 

  • Foyer CH (1993) Ascorbic acid. In: Alscher RG, Hess JL (eds) Antioxidants in higher plants. CRC, Boca Raton, pp 31–58

    Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    PubMed  CAS  Google Scholar 

  • Foyer CH, Halliwell B (1977) Purification and properties of dehydroascorbate reductase from spinach leaves on the growth of hybrid poplar. Plant Dis 66:587–589

    Google Scholar 

  • Foyer CH, Mullineaux PM (1998) The presence of dehydroascorbate and dehydroascorbate reductase in plant tissues. FEBS Lett 425:528–529

    PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    CAS  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    PubMed  CAS  PubMed Central  Google Scholar 

  • Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100

    PubMed  CAS  PubMed Central  Google Scholar 

  • Frei M, Wissuwa M, Pariasca-Tanaka J, Chen CP, Südekum K-H, Kohno Y (2012) Leaf ascorbic acid level—is it really important for ozone tolerance in rice? Plant Physiol Biochem 59:63–70

    PubMed  CAS  Google Scholar 

  • Gajewska E, Sklodowska M (2008) Differential biochemical responses of wheat shoots and roots to nickel stress: antioxidative reactions and proline accumulation. Plant Growth Regul 54:179–188

    CAS  Google Scholar 

  • Gatzek S, Wheeler GL, Smirnoff N (2002) Antisense suppression of L-galactose dehydrogenase in Arabidopsis thaliana provides evidence for its role in ascorbate synthesis and reveals light modulated L-galactose synthesis. Plant J 30:541–553

    PubMed  CAS  Google Scholar 

  • Gest N, Gautier H, Stevens R (2012) Ascorbate as seen through plant evolution: the rise of a successful molecule? J Exp Bot 64:33–53

    PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    PubMed  CAS  Google Scholar 

  • Hasanuzzaman M, Fujita M (2011) Selenium pretreatment upregulates the antioxidant defense and methylglyoxal detoxification system and confers enhanced tolerance to drought stress in rapeseed seedlings. Biol Trace Elem Res 143:1758–1776

    PubMed  CAS  Google Scholar 

  • Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicol 22:584–596

    CAS  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2010) Physiological and biochemical mechanisms of nitric oxide induced abiotic stress tolerance in plants. Am J Plant Physiol 5:295–324

    CAS  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2011a) Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol Rep 5:353–365

    Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2011b) Selenium-induced up-regulation of the antioxidant defense and methylglyoxal detoxification system reduces salinity-induced damage in rapeseed seedlings. Biol Trace Elem Res 143:1704–1721

    PubMed  CAS  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2012a) Exogenous selenium pretreatment protects rapeseed seedlings from cadmium-induced oxidative stress by upregulating the antioxidant defense and methylglyoxal detoxification systems. Biol Trace Elem Res 149:248–261

    PubMed  CAS  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Teixeira da Silva JA, Fujita M (2012b) Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Venkateshwarulu B, Shanker AK, Shanker C, Mandapaka M (eds) Crop stress and its management: perspectives and strategies. Springer, Berlin, pp 261–316

    Google Scholar 

  • Hasanuzzaman M, Nahar K, Alam MM, Fujita M (2012c) Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum) seedlings by modulating the antioxidant defense and glyoxalase system. Aust J Crop Sci 6:1314–1323

    CAS  Google Scholar 

  • Hatata MM, Abdel-Aal EA (2008) Oxidative stress and antioxidant defence mechanisms in response to cadmium treatments. Am Eurasian J Agric Environ Sci 4:655–669

    Google Scholar 

  • Hegedus A, Erdei S, Horvath G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci 160:1085–1093

    PubMed  CAS  Google Scholar 

  • Herschbach C, Scheerer U, Rennenberg H (2010) Redox states of glutathione and ascorbate in root tips of poplar (Populus tremula × P. alba) depend on phloem transport from the shoot to the roots. J Exp Bot 61:1065–1074

    PubMed  CAS  PubMed Central  Google Scholar 

  • Horemans N, Asard H, Caubergs RJ (1997) The ascorbate carrier of higher plant plasma membranes preferentially translocates the fully oxidized (dehydroascorbate) molecule. Plant Physiol 114:1247–1253

    PubMed  CAS  PubMed Central  Google Scholar 

  • Horemans N, Asard H, Caubergs RJ (1998) Carrier mediated uptake of dehydroascorbate into higher plant plasma membrane vesicles shows trans-stimulation. FEBS Lett 421:41–44

    PubMed  CAS  Google Scholar 

  • Horemans N, Foyer CH, Asard H (2000) Transport and action of ascorbate at the plant plasma membrane. Trend Plant Sci 5:263–267

    CAS  Google Scholar 

  • Horemans N, Raeymaekers T, Beek KV, Nowocin A, Blust R, Broos K, Cuypers A et al (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 

  • Hossain MA, Asada K (1985) Monodehydroascorbate reductase from cucumber is a flavin adenine dinucleotide enzyme. J Biol Chem 260:12920–12926

    PubMed  CAS  Google Scholar 

  • Hossain MA, Fujita M (2012) Regulatory role of components of ascorbate-glutathione (AsA-GSH) pathway in plant tolerance to oxidative stress. In: Anjum NA, Umar S, Ahmed A (eds) Oxidative stress in plants: causes, consequences and tolerance. IK International Publishing House, New Delhi, pp 81–147

  • Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in the regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385–395

    CAS  Google Scholar 

  • Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plant 16:259–272

    CAS  Google Scholar 

  • Imai T, Karita S, Shiratori G, Hattori M, Nunome T, Oba K et al (1998) L-Galactono-gamma-lactone dehydrogenase from sweet potato: purification and cDNA sequence analysis. Plant Cell Physiol 39:1350–1358

    PubMed  CAS  Google Scholar 

  • Iqbal N, Masood A, Nazar R, Syeed S, Khan NA (2010) Photosynthesis, growth and antioxidant metabolism in mustard (Brassica juncea L.) cultivars differing in cadmium tolerance. Agric Sci China 9:519–527

    CAS  Google Scholar 

  • Ishikawa T, Shigeoka S (2008) Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem 72:1143–1154

    PubMed  CAS  Google Scholar 

  • Ishikawa T, Yoshimura K, Sakai K, Tamoi M, Takeda T, Shigeoka S (1998) Molecular characterization and physiological role of a glyoxysome-bound ascorbate peroxidase from spinach. Plant Cell Physiol 39:23–34

    PubMed  CAS  Google Scholar 

  • Ishikawa T, Dowdle J, Smirnoff N (2006) Progress in manipulating ascorbic acid biosynthesis and accumulation in plants. Physiol Plant 126:343–355

    CAS  Google Scholar 

  • Islam MM, Hoque MA, Okuma E, Jannat R, Banu MNA, Jahan MS et al (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 

  • Israr M, Sahi SV, Jain J (2006) Cadmium accumulation and antioxidative responses in the Sesbania drumondiiallus. Arch Environ Contam Toxicol 50:121–127

    PubMed  CAS  Google Scholar 

  • Israr M, Jewell A, Kumar D, Sahi SV (2011) Interactive effects of lead, copper, nickel and zinc on growth, metal uptake and antioxidative metabolism of Sesbania drummondii. J Hazard Mater 186:1520–1526

    PubMed  CAS  Google Scholar 

  • Jiménez A, Hernández JA, Del Rio LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284

    PubMed  PubMed Central  Google Scholar 

  • Jin X, Yang X, Mahmood Q, Islam E, Liu D, Li H (2008) Response of antioxidant enzymes, ascorbate and glutathione metabolism towards cadmium in hyperaccumulator and nonhyperaccumulator ecotypes of Sedum alfredii H. Environ Toxicol 23:517–529

    PubMed  CAS  Google Scholar 

  • Justi KC, Visentainer JV, deSouza NE, Matsushita M (2000) Nutritional composition and vitamin C stability in stored camu-camu (Myrciaria dubia) pulp. Arch Latinoam Nutr 50:405–408

    PubMed  CAS  Google Scholar 

  • Kanwar MK, Bhardwaj R, Arora P, Chowdhary SP, Sharma P, Kumar S (2012) Plant steroid hormones produced under Ni stress are involved in the regulation of metal uptake and oxidative stress in Brassica juncea L. Chemosphere 86:41–49

    PubMed  CAS  Google Scholar 

  • Karuppanapandian T, Manoharan K (2008) Uptake and translocation of tri- and hexa-valent chromium and their effects on black gram (Vigna mungo L. Hepper cv. Co4) Roots. J Plant Biol 51:192–201

    CAS  Google Scholar 

  • Karyotou K, Donaldson RP (2005) Ascorbate peroxidase, a scavenger of hydrogen peroxide in glyoxysomal membranes. Arch Biochem Biophys 434:248–257

    PubMed  CAS  Google Scholar 

  • Kato N, Esaka M (1999) Changes in ascorbate oxidase gene expression and ascorbate levels in cell division and cell elongation in tobacco cells. Physiol Plant 105:321–329

    CAS  Google Scholar 

  • Khan NA, Samiullah SS, Nazar R (2007) Activities of antioxidative enzymes, sulphur assimilation, photosynthetic activity and growth of wheat (Triticum aestivum) cultivars differing in yield potential under cadmium stress. J Agron Crop Sci 193:435–444

    CAS  Google Scholar 

  • Khan I, Ahmad A, Iqbal M (2009) Modulation of antioxidant defence system for arsenic detoxification in Indian mustard. Ecotoxicol Environ Saf 72:626–634

    PubMed  CAS  Google Scholar 

  • Kieselbach T, Bystedt M, Hynds P, Robinson C, Schröder WP (2000) A peroxidase homologue and novel plastocyanin located by proteomics to the Arabidopsis chloroplast thylakoid lumen. FEBS Lett 480:271–276

    PubMed  CAS  Google Scholar 

  • Kotchoni SO, Larrimore KE, Mukherjee M, Kempinski CF, Barth C (2009) Alterations in the endogenous ascorbic acid content affect flowering time in Arabidopsis. Plant Physiol 149:803–815

    PubMed  CAS  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  • Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol 165:920–931

    PubMed  CAS  Google Scholar 

  • Kwon SY, Choi SM, Ahn YO, Lee HS, Lee HB, Park YM, Kwak SS (2003) Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbate reductase gene. J Plant Physiol 160:347–353

    PubMed  CAS  Google Scholar 

  • Laing WA, Bulley S, Wright M, Cooney J, Jensen D, Barraclough D, MacRae E (2004) A highly specific L-galactose-1-phosphate phosphatase on the path to ascorbate biosynthesis. Proc Natl Acad Sci U S A 101:16976–16981

    PubMed  CAS  PubMed Central  Google Scholar 

  • Laing WA, Wright MA, Cooney J, Bulley SM (2007) The missing step of the L-galactose pathway of ascorbate biosynthesis in plants, an L-galactose guanyltransferase, increases leaf ascorbate content. Proc Natl Acad Sci U S A 104:9534–9539

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lamhamdi M, Bakrim A, Aarab A, Lafont R, Sayah F (2011) Effects of lead phytotoxicity on wheat (Triticum aestivum L.) seed germination and seedling growth. C R Biol 334:118–126

    PubMed  CAS  Google Scholar 

  • Lee YP, Kim SH, Bang JW, Lee HS, Kwak SS, Kwon SY (2007) Enhanced tolerance to oxidative stress in transgenic tobacco plants expressing three antioxidant enzymes in chloroplasts. Plant Cell Rep 26:591–598

    PubMed  CAS  Google Scholar 

  • Leterrier M, Corpas FJ, Barroso JB, Sandalio LM, del Rio LA (2005) Peroxisomal monodehydroascorbate reductase. Genomic clone characterization and functional analysis under environmental stress conditions. Plant Physiol 138:2111–2123

    PubMed  CAS  PubMed Central  Google Scholar 

  • Li M, Ma F, Guo C, Liu J (2010) Ascorbic acid formation and profiling of genes expressed in its synthesis and recycling in apple leaves of different ages. Plant Physiol Biochem 48:216–224

    PubMed  CAS  Google Scholar 

  • Li X, Ma H, Jia P, Wang J, Jia L, Zhang T, Yang Y, Chen H, Wei X (2012) Responses of seedling growth and antioxidant activity to excess iron and copper in Triticum aestivum L. Ecotoxicol Environ Saf 86:47–53

    PubMed  CAS  Google Scholar 

  • Linster CL, Clarke SG (2008) L-Ascorbate biosynthesis in higher plants: the role of VTC2. Trend Plant Sci 13:567–573

    CAS  Google Scholar 

  • Liso R, Innocenti AM, Bitonti MB, Arrigoni O (1988) Ascorbic acid-induced progression of quiescent center cells from G1 to S phase. New Phytol 110:469–471

    CAS  Google Scholar 

  • Liso R, De Tullio MC, Ciraci S, Balestrini R, La Rocca N et al (2004) Localisation of ascorbic acid, ascorbic acid oxidase, and glutathione in roots of Cucurbita maxima L. J Exp Bot 55:2589–2597

    PubMed  CAS  Google Scholar 

  • Liu X, Shiomi S, Nakatsuka A, Kubo Y, Nakamura R, Inaba A (1999) Characterization of ethylene biosynthesis associated with ripening in banana fruit. Plant Physiol 121:1257–1266

    PubMed  CAS  PubMed Central  Google Scholar 

  • Locato V, de Pinto MC, De Gara L (2009) Different involvement of the mitochondrial, plastidal and cytosolic ascorbate-glutathione redox enzymes in heat shock responses. Phyiol Plant 135:296–306

    CAS  Google Scholar 

  • Loewus FA (1999) Biosynthesis and metabolism of ascorbic acid in plants and of analogs of ascorbic acid in fungi. Phytochemistry 52:193–210

    CAS  Google Scholar 

  • Lopéz-Carbonell M, Munné-Bosch S, Alegre L (2006) The ascorbate-deficient vtc-1 Arabidopsis mutant shows altered ABA accumulation in leaves and chloroplast. J Plant Growth Regul 25:137–144

    Google Scholar 

  • Lorence A, Chevone BI, Mendes P, Nessler CL (2004) myo-Inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiol 134:1200–1205

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lunde C, Baumann U, Shirley NJ, Drew DP, Fincher GB (2006) Gene structure and expression pattern analysis of three monodehydroascorbate reductase (Mdhar) genes in Physcomitrella patens: implications for the evolution of the MDHAR family in plants. Plant Mol Biol 60:259–275

    PubMed  CAS  Google Scholar 

  • Lyubenova L, Schröder P (2011) Plants for waste water treatment—effects of heavy metals on the detoxification system of Typha latifolia. Bioresource Technol 102:996–1004

    CAS  Google Scholar 

  • Maheshwari R, Dubey RS (2009) Nickel-induced oxidative stress and the role of antioxidative defense in rice seedlings. Plant Growth Regul 59:37–49

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Mano J, Hideg E, Asada K (2004) Ascorbate in thylakoid lumen functions as an alternative electron donor to photosystem II and photosystem I. Arch Biochem Biophys 429:71–80

    PubMed  CAS  Google Scholar 

  • Markovska YK, Gorinova NI, Nedkovska MP, Miteva KM (2009) Cadmium-induced oxidative damage and antioxidant responses in Brassica juncea plants. Biol Plant 53:151–154

    CAS  Google Scholar 

  • Martínez JP, Araya H (2010) Ascorbate-glutathione cycle: enzymatic and non-enzymatic integrated mechanisms and its biomolecular regulation. In: Anjum NA, Chan MT, Umar S (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Dordrecht, pp 303–322

    Google Scholar 

  • Mathews MC, Summers CB, Felton GW (1997) Ascorbate peroxidase: a novel antioxidant enzyme in insects. Arch Insect Biochem Physiol 34:57–68

    CAS  Google Scholar 

  • Mishra S, Jha AB, Dubey RS (2011) Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma 248:565–577

    PubMed  CAS  Google Scholar 

  • Mittler R, Zilinskas BA (1991) Purification and characterization of pea cytosolic ascorbate peroxidase. Plant Physiol 97:962–968

    PubMed  CAS  PubMed Central  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trend Plant Sci 9:490–498

    CAS  Google Scholar 

  • Mittova V, Tal M, Volokita M, Guy M (2003) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ 26:845–856

    PubMed  CAS  Google Scholar 

  • Miyake C, Asada K (1992) Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol 33:541–553

    CAS  Google Scholar 

  • Miyake C, Asada K (1994) Ferredoxin-dependent photoreduction of the monodehydroascorbate radical in spinach thylakoids. Plant Cell Physiol 35:539–549

    CAS  Google Scholar 

  • Miyake C, Michihata F, Asada K (1991) Scavenging of hydrogen peroxide in prokaryotic and eukaryotic algae: acquisition of ascorbate peroxidase during the evolution of cyanobacteria. Plant Cell Physiol 32:33–43

    CAS  Google Scholar 

  • Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164:601–610

    PubMed  CAS  Google Scholar 

  • Mohamed AA, Castagna A, Ranieri A, Sanità di Toppi L (2012) Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis. Plant Physiol Biochem 57C:15–22

    Google Scholar 

  • Morell S, Follmann H, De Tullio M, Häberlein I (1997) Dehydroascorbate and dehydroascorbate reductase are phantom indicators of oxidative stress in plants. FEBS Lett 414:567–570

    PubMed  CAS  Google Scholar 

  • Mullen RT, Trelease RN (1996) Biogenesis and membrane properties of peroxisomes: does the boundary membrane serve and protect? Trend Plant Sci 1:389–394

    Google Scholar 

  • Mullineaux P, Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5:43–48

    PubMed  CAS  Google Scholar 

  • Murthy SS, Zilinskas BA (1994) Molecular cloning and characterization of a DNA encoding pea monodehydroascorbate reductase. J Biol Chem 269:31129–31133

    PubMed  CAS  Google Scholar 

  • Nehnevajova E, Lyubenova L, Herzig R, Schröder P, Schwitzguébel JP, Schmülling T (2012) Metal accumulation and response of antioxidant enzymes in seedlings and adult sunflower mutants with improved metal removal traits on a metal-contaminated soil. Environ Exp Bot 76:39–48

    CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    PubMed  CAS  Google Scholar 

  • Noctor G, Arisi ACM, Jouanin L, Kunert KJ, Rennenberg H, Foyer CH (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49:623–647

    CAS  Google Scholar 

  • Nouairi I, Ammar WB, Youssef NB, Miled DDB, Ghorbal MH, Zarrouk M (2009) Antioxidant defense system in leaves of Indian mustard (Brassica juncea) and rape (Brassica napus) under cadmium stress. Acta Physiol Plant 31:237–247

    CAS  Google Scholar 

  • Paciolla C, De Tullio MC, Chiappetta A, Innocenti AM, Bitonti MB, Liso R, Arrigoni O (2001) Short- and long-term effects of dehydroascorbate in Lupinus albus and Allium cepa roots. Plant Cell Physiol 42:857–863

    PubMed  CAS  Google Scholar 

  • Pang CH, Wang BS (2010) Role of ascorbate peroxidase and glutathione reductase in ascorbate-glutathione cycle and stress tolerance in plants. In: Anjum NA, Umar S, Chan MT (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Dordrecht, pp 91–112

    Google Scholar 

  • Paradiso A, Berardino R, De Pinto MC et al (2008) Increase in ascorbate-glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol 49:362–374

    PubMed  CAS  Google Scholar 

  • Parsons HT, Fry SC (2012) Oxidation of dehydroascorbic acid and 2,3-diketogulonate under plant apoplastic conditions. Phytochemistry 75:41–49

    PubMed  CAS  Google Scholar 

  • Parsons HT, Yasmin T, Fry SC (2011) Alternative pathways of dehydroascorbic acid degradation in vitro and in plant cell cultures: novel insights into vitamin C catabolism. Biochem J 440:375–383

    PubMed  CAS  Google Scholar 

  • Pastori GM, Foyer CH (2002) Common components, networks and pathways of cross tolerance to stress: the central role of ‘redox’ and ABA-mediated controls. Plant Physiol 129:460–468

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S et al (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell Online 15:939–951

    CAS  Google Scholar 

  • Pekker I, Tel-Or E, Mittler R (2002) Reactive oxygen intermediates and glutathione regulate the expression of cytosolic ascorbate peroxidase during iron-mediated oxidative stress in bean. Plant Mol Biol 49:429–438

    PubMed  CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. doi:10.1155/2012/217037

    Google Scholar 

  • Pignocchi C, Kiddle G, Hernández I, Foster SJ, Asensi A et al (2006) Ascorbate oxidase-dependent changes in the redox state of the apoplast modulate gene transcript accumulation leading to modified hormone signaling and orchestration of defense processes in tobacco. Plant Physiol 141:423–435

    PubMed  CAS  PubMed Central  Google Scholar 

  • Polle A (2001) Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modeling—computer simulations as a step towards flux analysis. Plant Physiol 126:445–462

    PubMed  CAS  PubMed Central  Google Scholar 

  • Posmyk MM, Kontek R, Janas KM (2009) Antioxidant enzymes activity and phenolic compounds content in red cabbage seedlings exposed to copper stress. Ecotoxicol Environ Saf 72:596–602

    PubMed  CAS  Google Scholar 

  • Potters G, Horemans N, Caubergs RJ, Asard H (2000) Ascorbate and dehydroascorbate influence cell cycle progression in tobacco cell suspension. Plant Physiol 124:17–20

    PubMed  CAS  PubMed Central  Google Scholar 

  • Potters G, De Gara L, Asard H, Horemans N (2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiol Biochem 40:537–548

    CAS  Google Scholar 

  • Potters G, Horemans N, Bellone S, Caubergs RJ, Trost P, Guisez Y, Asard H (2004) Dehydroascorbate influences the plant cell cycle through a glutathione-independent reduction mechanism. Plant Physiol 134:1479–1487

    PubMed  CAS  PubMed Central  Google Scholar 

  • Potters G, Horemans N, Jansen MAK (2010) The cellular redox state in plant stress biology—a charging concept. Plant Physiol Biochem 48:292–300

    PubMed  CAS  Google Scholar 

  • Pourcel L, Routaboul JM, Cheynier V (2007) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trend Plant Sci 12:29–36

    CAS  Google Scholar 

  • Prasad MNV (2004) Heavy metal stress in plants: from biomolecules to ecosystems, 2nd edn. Springer, Berlin

    Google Scholar 

  • Qureshi MI, Israr M, Abdin MZ, Iqbal M (2005) Responses of Artemisia annua L. to lead and salt-induced oxidative stress. Environ Exp Bot 53:185–193

    CAS  Google Scholar 

  • Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Barr JE et al (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J 32:329–342

    PubMed  CAS  Google Scholar 

  • Romero-Puertas MC, Corpas FJ, Rodriguez-Serrano M, Gomez M et al (2007) Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. J Plant Physiol 164:1346–1357

    PubMed  CAS  Google Scholar 

  • Rosa SB, Caverzan A, Teixeira FK, Lazzarotto F, Silveira JA et al (2010) Cytosolic APx knockdown indicates an ambiguous redox responses in rice. Phytochemistry 71:548–558

    PubMed  CAS  Google Scholar 

  • Saeidi-Sar S, Khavari-Nejad RA, Fahimi H, Ghorbanli M, Majd A (2007) Interactive effects of gibberellin A3 and ascorbic acid on lipid peroxidation and antioxidant enzyme activities in Glycine max seedlings under nickel stress. Russ J Plant Physiol 54:74–79

    CAS  Google Scholar 

  • Sakihama Y, Mano JI, Sano S, Asada K, Yamasaki H (2000) Reduction of phenoxyl radicals mediated by monodehydroascorbate reductase. Biochem Biophys Res Commun 279:949–954

    PubMed  CAS  Google Scholar 

  • Sanmartin M, Drogoudi P, Lyons T, Pateraki I, Barnes J, Kanellis A (2003) Overexpression of ascorbate oxidase in the apoplast of transgenic tobacco results in altered ascorbate and glutathione redox states and increased sensitivity to ozone. Planta 216:918–928

    PubMed  CAS  Google Scholar 

  • Sano S, Ueda M, Kitajima S, Takeda T, Shigeoka S et al (2001) Characterization of ascorbate peroxidases from unicellular red alga Galdieria partita. Plant Cell Physiol 42:433–440

    PubMed  CAS  Google Scholar 

  • Sano S, Tao S, Endo Y, Inaba T, Hossain MA et al (2005) Purification and cDNA cloning of chloroplastic monodehydroascorbate reductase from spinach. Biosci Biotechnol Biochem 69:762–772

    PubMed  CAS  Google Scholar 

  • Scandalios JG (2002) The rise of ROS. Trends Biochem Sci 27:483–486

    PubMed  CAS  Google Scholar 

  • Schröder P, Lyudmila L, Huber C (2009) Do heavy metals and metalloids influence the detoxification of organic xenobiotics in plants? Environ Sci Pollut Res 16:795–804

    Google Scholar 

  • Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R et al (2001) Cadmium-induced changes in antioxidative systems, H2O2 content and differentiation in pine (Pinus sylvestris) roots. Plant Physiol 127:887–898

    PubMed  PubMed Central  Google Scholar 

  • Schützendübel A, Nikolova P, Rudolf C, Polle A (2002) Cadmium and H2O2 induced oxidative stress in Populas × canescens roots. Plant Physiol Biochem 40:577–584

    Google Scholar 

  • Sharma P, Dubey RS (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminium. Plant Cell Rep 26:2027–2038

    PubMed  CAS  Google Scholar 

  • Shen GM, Zhu C, Shangguan LN, Du QZ (2012) The Cd-tolerant rice mutant cadH-5 is a high Cd accumulator and shows enhanced antioxidant activity. J Plant Nutr Soil Sci 175:309–318

    CAS  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    PubMed  CAS  Google Scholar 

  • Shimaoka T, Yokota A, Miyake C (2000) Purification and characterization of chloroplast dehydroascorbate reductase from spinach leaves. Plant Cell Physiol 41:1110–1118

    PubMed  CAS  Google Scholar 

  • Siendones E, Gonzales-Reyes JA, Santos-Ocana C, Navas P, Cordoba F (1999) Biosynthesis of ascorbic acid in kidney bean. L-galactono-γ-lactone dehydrogenase is an intrinsic protein located at the mitochondrial inner membrane. Plant Physiol 120:907–912

    PubMed  CAS  PubMed Central  Google Scholar 

  • Singh S, Khan NA, Nazar R, Anjum NA (2008) Photosynthetic traits and activities of antioxidant enzymes in blackgram (Vigna mungo L. Hepper) under cadmium stress. Am J Plant Physiol 3:25–32

    CAS  Google Scholar 

  • Singh R, Gautam N, Mishra A, Gupta R (2011) Heavy metals and living systems: an overview. Indian J Pharmacol 43:246–53

    PubMed  CAS  PubMed Central  Google Scholar 

  • Singh VP, Srivastava PK, Prasad SM (2013) Nitric oxide alleviates arsenic-induced toxic effects in ridged Luffa seedlings. Plant Physiol Biochem 71:155–163

    PubMed  CAS  Google Scholar 

  • Smirnoff N (1996) The function and metabolism of ascorbic acid in plants. Ann Bot 78:661–669

    CAS  Google Scholar 

  • Smirnoff N (2000) Ascorbate biosynthesis and function in photoprotection. PhilTrans Royal Soc London B 355:1455–1464

    CAS  Google Scholar 

  • Smirnoff N (2011) Vitamin C: the metabolism and functions of ascorbic acid in plants. Adv Bot Res 59:107–177

    CAS  Google Scholar 

  • Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Critic Rev Biochem Mol Biol 35:291–314

    CAS  Google Scholar 

  • Smirnoff N, Conklin PL, Loewus FA (2001) Biosynthesis of ascorbic acids in plants: a renaissance. Annu Rev Plant Physiol Plant Mol Biol 52:437–467

    PubMed  CAS  Google Scholar 

  • Sobrino-Plata J, Ortega-Villasante C, Flores-Caceres ML, Escobar C, Del Campo FF, Hernandez LE (2009) Differential alterations of antioxidant defenses as bioindicators of mercury and cadmium toxicity in alfalfa. Chemosphere 77:946–954

    PubMed  CAS  Google Scholar 

  • Sytar O, Kumar A, Latowski D, Kuczynska P, Strzałka K, Prasad MNV (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999

    CAS  Google Scholar 

  • Takahama U, Oniki T (1992) Regulation of peroxidase-dependent oxidation of phenolics in the apoplast of spinach leaves by ascorbate. Plant Cell Physiol 33:379–387

    CAS  Google Scholar 

  • Takeda T, Yoshimura K, Ishikawa T, Shigeoka S (1998) Purification and characterization of ascorbate peroxidase in Chlorella vulgaris. Biochimie 80:295–301

    PubMed  CAS  Google Scholar 

  • Talukdar T, Talukdar D (2013) Response of antioxidative enzymes to arsenic-induced phytotoxicity in leaves of a medicinal daisy, Wedelia chinensis Merrill. J Nat Sci Biol Med 4:383–388

    PubMed  CAS  PubMed Central  Google Scholar 

  • Teixeira FK, Menezes-Benavente L, Galvão VC, Margis R, Margis-Pinheiro M (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 224:300–314

    PubMed  CAS  Google Scholar 

  • Tewari RK, Parma PK, Sharma N (2006) Antioxidant responses to enhanced generation of superoxide anion radical and hydrogen peroxide in the copper-stressed mulberry plants. Planta 223:1145–1153

    PubMed  CAS  Google Scholar 

  • Thounaojam TC, Panda P, Mazumdar P, Kumar D, Sharma GD et al (2012) Excess copper induced oxidative stress and response of antioxidants in rice. Plant Physiol Biochem 53:33–39

    PubMed  CAS  Google Scholar 

  • Touiserkani T, Haddad R (2012) Cadmium-induced stress and antioxidative responses in different Brassica napus cultivars. J Agr Sci Tech 14:929–937

    CAS  Google Scholar 

  • Tripathi P, Mishra A, Dwivedi S, Chakrabarty D, Trivedi PK, Singh RP, Tripathi RD (2012) Differential response of oxidative stress and thiol metabolism in contrasting rice genotypes for arsenic tolerance. Ecotoxicol Environ Saf 79:189–198

    PubMed  CAS  Google Scholar 

  • Wada N, Kinoshita S, Matsuo M, Amako K, Miyake C, Asada K (1998) Purification and molecular properties of ascorbate peroxidase from bovine eye. Biochem Biophys Res Commun 242:256–261

    PubMed  CAS  Google Scholar 

  • Wang H, Feng T, Peng X, Yan M, Tang X (2009) Up-regulation of chloroplastic antioxidant capacity is involved in alleviation of nickel toxicity of Zea mays L. by exogenous salicylic acid. Ecotoxicol Environ Saf 72:1354–62

    PubMed  CAS  Google Scholar 

  • Wang Z, Xiao Y, Chen W, Tang K, Zhang L (2010) Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis. J Integ Plant Biol 52:400–409

    CAS  Google Scholar 

  • Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369

    PubMed  CAS  Google Scholar 

  • Wolucka BA, VanMontagu M (2003) GDP-D-mannose 300,500-epimerase forms GDP-L-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants. J Biol Chem 278:47483–47490

    PubMed  CAS  Google Scholar 

  • Wu FB, Chen F, Wei K, Zhang GP (2004) Effect of cadmium on free amino acid, glutathione and ascorbic acid concentrations in two barley genotypes (Hordeum vulgare L.) differing in cadmium tolerance. Chemosphere 57:447–454

    PubMed  CAS  Google Scholar 

  • Yamaguchi K, Mori H, Nishimura M (1995) A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin. Plant Cell Physiol 36:1157–1162

    PubMed  CAS  Google Scholar 

  • Yin L, Wang S, Eltayeb AE, Uddin MI, Yamamoto Y et al (2010) Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231:609–621

    PubMed  CAS  Google Scholar 

  • Yoon HS, Lee H, Lee IA, Kim KY, Jo JK (2004) Molecular cloning of the monodehydroascorbate reductase gene from Brassica campestris and analysis of its mRNA level in response to oxidative stress. Biochim Biophys Acta Bioenerg 1658:181–186

    CAS  Google Scholar 

  • Yoshida S, Tamaoki M, Shikano T, Nakajima N, Ogawa D, Ioki M, Aono M, Kubo A, Kamada H, Inoue Y, Saji H (2006) Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana. Plant Cell Physiol 47:304–308

    PubMed  CAS  Google Scholar 

  • Zelinová V, Bočová B, Huttová J, Mistrík I, Tamás L (2013) Impact of cadmium and hydrogen peroxide on ascorbate-glutathione recycling enzymes in barley root. Plant Soil Environ 59:62–67

    Google Scholar 

  • Zhang FQ, Shi WY, Jin ZX, Shen ZG (2003) Response of antioxidative enzymes in cucumber chloroplast to cadmium toxicity. J Plant Nutr 26:1779–1788

    CAS  Google Scholar 

  • Zhao ZQ, Cai YL, Zhu YG, 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 168:759–763

    CAS  Google Scholar 

Download references

Acknowledgments

NAA (SFRH/BPD/84671/2012), ACD, EP, and IA are grateful to the Portuguese Foundation for Science and Technology (FCT) and the Aveiro University Research Institute/Centre for Environmental and Marine Studies (CESAM) for partial financial support. SSG, RG, RT and NT acknowledge the funds from CSIR, DST, and UGC, Government of India, New Delhi. The authors apologize if some references related to the main theme of the current article could not be cited due to space constraint.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Centre for Environmental and Marine Studies (CESAM) and Department of Chemistry, University of Aveiro, 3810-193, Aveiro, Portugal

    Naser A. Anjum, Armando C. Duarte, Eduarda Pereira & Iqbal Ahmad

  2. Centre for Environmental and Marine Studies (CESAM) and Department of Biology, University of Aveiro, 3810-193, Aveiro, Portugal

    Iqbal Ahmad

  3. Stress Physiology and Molecular Biology Lab, Centre for Biotechnology, MD University, Rohtak, 001, India

    Sarvajeet S. Gill & Ritu Gill

  4. Department of Agronomy, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Dhaka, 1207, Bangladesh

    Mirza Hasanuzzaman

  5. International Centre for Genetic Engineering and Biotechnology (ICGEB), Aruna Asaf Ali Marg, New Delhi, 067, India

    Renu Tuteja & Narendra Tuteja

Authors
  1. Naser A. Anjum
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarvajeet S. Gill
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ritu Gill
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mirza Hasanuzzaman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Armando C. Duarte
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eduarda Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Iqbal Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Renu Tuteja
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Narendra Tuteja
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Naser A. Anjum, Iqbal Ahmad or Narendra Tuteja.

Additional information

Handling Editor: David Robinson

Rights and permissions

Reprints and permissions

About this article

Cite this article

Anjum, N.A., Gill, S.S., Gill, R. et al. Metal/metalloid stress tolerance in plants: role of ascorbate, its redox couple, and associated enzymes. Protoplasma 251, 1265–1283 (2014). https://doi.org/10.1007/s00709-014-0636-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-014-0636-x

Keywords

Search

Navigation