Environmental Science and Pollution Research

, Volume 23, Issue 19, pp 19002–19029 | Cite as

Catalase and ascorbate peroxidase—representative H2O2-detoxifying heme enzymes in plants

  • Naser A. AnjumEmail author
  • Pallavi SharmaEmail author
  • Sarvajeet S. Gill
  • Mirza Hasanuzzaman
  • Ekhlaque A. Khan
  • Kiran Kachhap
  • Amal A. Mohamed
  • Palaniswamy Thangavel
  • Gurumayum Devmanjuri Devi
  • Palanisamy Vasudhevan
  • Adriano Sofo
  • Nafees A. Khan
  • Amarendra Narayan MisraEmail author
  • Alexander S. Lukatkin
  • Harminder Pal Singh
  • Eduarda Pereira
  • Narendra TutejaEmail author
Review Article


Plants have to counteract unavoidable stress-caused anomalies such as oxidative stress to sustain their lives and serve heterotrophic organisms including humans. Among major enzymatic antioxidants, catalase (CAT; EC and ascorbate peroxidase (APX; EC are representative heme enzymes meant for metabolizing stress-provoked reactive oxygen species (ROS; such as H2O2) and controlling their potential impacts on cellular metabolism and functions. CAT mainly occurs in peroxisomes and catalyzes the dismutation reaction without requiring any reductant; whereas, APX has a higher affinity for H2O2 and utilizes ascorbate (AsA) as specific electron donor for the reduction of H2O2 into H2O in organelles including chloroplasts, cytosol, mitochondria, and peroxisomes. Literature is extensive on the glutathione-associated H2O2-metabolizing systems in plants. However, discussion is meager or scattered in the literature available on the biochemical and genomic characterization as well as techniques for the assays of CAT and APX and their modulation in plants under abiotic stresses. This paper aims (a) to introduce oxidative stress-causative factors and highlights their relationship with abiotic stresses in plants; (b) to overview structure, occurrence, and significance of CAT and APX in plants; (c) to summarize the principles of current technologies used to assay CAT and APX in plants; (d) to appraise available literature on the modulation of CAT and APX in plants under major abiotic stresses; and finally, (e) to consider a brief cross-talk on the CAT and APX, and this also highlights the aspects unexplored so far.


Abiotic stress Reactive oxygen species Oxidative stress Catalase Ascorbate peroxidase Plant stress tolerance 



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


  1. Abler ML, Scandalios JG (1993) Isolation and characterization of a genomic sequence encoding the maize Cat3 catalase gene. Plant Mol Biol 22:1031–1038CrossRefGoogle Scholar
  2. Aebi H (1984) Catalase. Methods Enzymol 105:121–126CrossRefGoogle Scholar
  3. Aebi H, Sutter H (1971) A catalasemia. Adv Hum Genet 2:143–199Google Scholar
  4. Agami RA, Mohamed GF (2013) Exogenous treatment with indole-3-acetic acid and salicylic acid alleviates cadmium toxicity in wheat seedlings. Ecotoxicol Environ Saf 94:164–171CrossRefGoogle Scholar
  5. Ahmad P, Nabi G, Ashraf M (2011) Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) Czern.& Coss.] plants can be alleviated by salicylic acid. South Afr J Bot 77:36–44CrossRefGoogle Scholar
  6. Alam MM, Hasanuzzaman M, Nahar K, Fujita M (2013) Exogenous salicylic acid ameliorates short-term drought stress in mustard (Brassica juncea L.) seedlings by up-regulating the antioxidant defense and glyoxalase system. Aust J Crop Sci 7:1053–1063Google Scholar
  7. Alam MM, Nahar K, Hasanuzzaman M, Fujita M (2014a) Alleviation of osmotic stress in Brassica napus, B. campestris, and B. juncea by ascorbic acid application. Biol Plant 58:697–708CrossRefGoogle Scholar
  8. Alam MM, Nahar K, Hasanuzzaman M, Fujita M (2014b) Exogenous jasmonic acid modulates the physiology, antioxidant defense and glyoxalase systems in imparting drought stress tolerance in different Brassica species. Plant Biotechnol Rep 8:279–293CrossRefGoogle Scholar
  9. Alam MM, Nahar K, Hasanuzzaman M, Fujita M (2014c) Trehalose-induced drought stress tolerance: a comparative study among different Brassica species. Plant Omics J 7:271–283Google Scholar
  10. Anjum NA, Umar S, Chan MT (2010) Ascorbate-glutathione pathway and stress tolerance in plants. Springer Science & Business Media, The NetherlandsGoogle Scholar
  11. Anjum NA, Aref IM, Duarte AC, Pereira E, et al. (2014a) Glutathione and proline can coordinately make plants withstand the joint attack of metal(loid) and salinity stresses. Front Plant Sci 5:662CrossRefGoogle Scholar
  12. Anjum NA, Gill SS, Gill R, Hasanuzzaman M, Duarte AC, et al. (2014b) Metal/metalloid stress tolerance in plants: role of ascorbate, its redox couple, and associated enzymes. Protoplasma 251:165–1283CrossRefGoogle Scholar
  13. Anjum NA, Singh HP, Khan MIR, Masood A, Per TS, et al. (2015) Too much is bad-an appraisal of phytotoxicity of elevated plant-beneficial heavy metal ions. Environ Sci Pollut Res 22:3361–3382CrossRefGoogle Scholar
  14. Arabaci G (2011) Partial purification and some properties of catalase from dill (Anethum graveolens L.). J Bio Life Sci 2:11–15Google Scholar
  15. 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 43:107–116CrossRefGoogle Scholar
  16. Artenie V, Tanase E (1981) Practicum de biochimie generala, 1981. Editura Univ Al. I Cuza, Iasi, pp. 233–239Google Scholar
  17. Asada K (1999) The water-water cycle in chloroplasts, scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639CrossRefGoogle Scholar
  18. Azpilicueta CE, Benavides MP, Tomaro ML, Gallego SM (2007) Mechanism of CATA3 induction by cadmium in sunflower leaves. Plant Physiol Biochem 45:589–595CrossRefGoogle Scholar
  19. 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 28:497–504Google Scholar
  20. Battistuzzi G, D’Onofrio M, Loschi L, Sola M (2001) Isolation and characterization of two peroxidases from Cucumis sativus. Arch Biochem Biophys 388:100–112CrossRefGoogle Scholar
  21. Begara-Morales JC, Sanchez-Calvo B, Chaki M, Valderrama R, et al. (2014) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538CrossRefGoogle Scholar
  22. Benecky MJ, Frew JE, Scowen N, Jones P, Hoffman BM (1993) EPR and ENDOR detection of compound I from Micrococcus lysodeikticus catalase. Biochemistry 32:1929–1933CrossRefGoogle Scholar
  23. Breidenbach RW, Kahn A, Beevers H (1968) Characterization of glycosomes from castor bean endosperm. Plant Physiol 43:705–713CrossRefGoogle Scholar
  24. Bunkelmann JR, Trelease RN (1996) Ascorbate peroxidase, a prominent membrane protein in oilseed glyoxysomes. Plant Physiol 110:589–598CrossRefGoogle Scholar
  25. Bursey EH, Poulos TL (2000) Two substrate binding sites in ascorbate peroxidase, the role of arginine 172. Biochemistry 27:7374–737Google Scholar
  26. 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 35:1011–1019CrossRefGoogle Scholar
  27. Celik A, Cullis PM, Sutcliffe MJ, Sangar R, Raven EL (2001) Engineering the active site of ascorbate peroxidase. Eur J Biochem 268:78–85Google Scholar
  28. Chaturvedi AK, Patel MK, Mishra A, Tiwari V, Jha B (2014) The SbMT-2 gene from a halophyte confers abiotic stress tolerance and modulates ROS scavenging in transgenic tobacco. PLoS One 9(10):e111379CrossRefGoogle Scholar
  29. Chen GX, Asada K (1989) APX in tea leaves, occurrence of two isoenzymes, the differences in their enzymatic and molecular properties. Plant Cell Physiol 30:987–998Google Scholar
  30. 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 48:663–672CrossRefGoogle Scholar
  31. Chew O, Whelan J, Millar H (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877CrossRefGoogle Scholar
  32. Chiang HC, Lo JC, Yeh KC (2006) Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environ Sci Technol 40:6792–6798CrossRefGoogle Scholar
  33. Collén J, Pinto E, Pedersén M, Colepicolo P (2003) Induction of oxidative stress in the red macroalga Gracilariatenuistipitata by pollutant metals. Arch Environ Contam Toxicol 45:337–342CrossRefGoogle Scholar
  34. Cong M, Lv J, Liu X, Zhao J, Wu H (2013) Gene expression responses in Suaeda salsa after cadmium exposure. Springer Plus 2:232CrossRefGoogle Scholar
  35. Corpas FJ (2015) What is the role of hydrogen peroxide in plant peroxisomes? Plant Biol (Stuttg) 17(6):1099–1103CrossRefGoogle Scholar
  36. Corpas FJ, Trelease RN (1998) Differential expression of ascorbate peroxidase, a putative molecular chaperone in the boundary membrane of differentiating cucumber seedling peroxisomes. J Plant Physiol 153:332–338CrossRefGoogle Scholar
  37. Corpas FJ, Bunkelmann J, Trelease RN (1994) Identification and immunochemical characterization of a family of peroxisome membrane proteins (PMPs) in oilseed glyoxysomes. Eur J Cell Biol 65:280–290Google Scholar
  38. Correa-Aragunde N, Foresi N, Delledonne M, Lamattina L (2013) Auxin induces redox regulation of ascorbate peroxidase 1 activity by S-nitrosylation/denitrosylation balance resulting in changes of root growth pattern in Arabidopsis. J Exp Bot 64:3339–3349CrossRefGoogle Scholar
  39. Cuypers A, Karen S, Jos R, Kelly O, Els K, Tony R, et al. (2011) The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol 168:309–316CrossRefGoogle Scholar
  40. D’Arcy-Lameta A, Ferrari-Iliou R, Contour-Ansel D, Pham-Thi AT, Zuily-Fodil Y (2006) Isolation and characterization of four ascorbate peroxidase cDNAs responsive to water deficit in cowpea leaves. Ann Bot 97:133–140CrossRefGoogle Scholar
  41. Dalton DA, Baird LM, Langeberg L, Taugher CY, Anyan WR, et al. (1993) Subcellular localization of oxygen defense enzymes in soybean (Glycine max [L.]Merr.) root nodules. Plant Physiol 102:481–489Google Scholar
  42. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, et al. (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268–281CrossRefGoogle Scholar
  43. De Leonardis S, Dipierro N, Dipierro S (2000) Purification and characterization of an APX from potato tuber mitochondria. Plant Physiol Biochem 38:773–779CrossRefGoogle Scholar
  44. De Pinto MC, Locato V, Sgobba A, Romero-PuertasMdel C, Gadaleta C, Delledonne M, De Gara L (2013) S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco Bright Yellow-2 cells. Plant Physiol 163:1766–1775CrossRefGoogle Scholar
  45. Deisseroth A, Dounce AL (1970) Catalase—physical and chemical properties, mechanism of catalysis and physiological role. Physiol Rev 50:319–375Google Scholar
  46. Del Río LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66(10):2827–2837CrossRefGoogle Scholar
  47. Del Rio LA, Mez Ortega MG, Leal Lopez A, Gorge J (1977) A more sensitive modification of the catalase assay with the Clark oxygen electrode application to the kinetic study of the pea leaf enzyme. Anal Biochem 80:409–415CrossRefGoogle Scholar
  48. Dong C, Zheng XF, Li GL, Pan C, Zhou MQ, Hu ZL (2011) Cloning and expression of one chloroplastic ascorbate peroxidase gene from Nelumbo nucifera. Biochem Genet 49:656–664CrossRefGoogle Scholar
  49. Dounce AL (1983) A proposed mechanism for the catalytic action of catalase. J Theor Biol 105:553–567CrossRefGoogle Scholar
  50. Drążkiewicz M, Skórzyńska-Polit E, Krupa Z (2010) Effect of BSO-supplemented heavy metals on antioxidant enzymes in Arabidopsis thaliana. Ecotoxicol Environ Saf 73:1362–1369CrossRefGoogle Scholar
  51. Du YY, Wang PC, Chen J, Song CP (2008) Comprehensive functional analysis of the catalase gene family in Arabidopsis thaliana. J Integr Plant Biol 50:1318–1326CrossRefGoogle Scholar
  52. Dynan WS, Tjian R (1985) Control of eukaryotic messenger RNA synthesis by sequence-specific DNA-binding proteins. Nature 316:774–778CrossRefGoogle Scholar
  53. Eising R, Gerhardt B (1987) Catalase degradation in sunflower cotyledons during peroxisome transition from glyoxysomal to leaf peroxisomal function. Plant Physiol 84:225–232CrossRefGoogle Scholar
  54. Eising R, Süselbeck B (1991) A density labelling method for the quantitation of radioactive label recycling in studies on individual protein turnover. J Exp Bot 42:947–955CrossRefGoogle Scholar
  55. El-Beltagi HS, Mohamed HI (2013) Alleviation of cadmium toxicity in Pisumsativum L. seedlings by calcium chloride. Not Bot Horti Agrobot 41:157–168Google Scholar
  56. El-Beltagi HS, Mohamed AA, Ashed MMR (2010) Response of antioxidative enzymes to cadmium stress in leaves and roots of radish (Raphanus sativus L.). Not Sci Biol 2:76–82Google Scholar
  57. Engel N, Schmidt M, Lutz C, Feierabend J (2006) Molecular identification, heterologous expression and properties of light-insensitive plant catalases. Plant Cell Environ 29:593–607CrossRefGoogle Scholar
  58. Eyidogan F, Oz MT (2005) Effect of salinity on antioxidant responses of chickpea seedlings. Acta Physiol Plant 29:485–493CrossRefGoogle Scholar
  59. Feierabend J, Schaan C, Hertwig B (1992) Photoinactivation of catalase occurs under both high and low temperature stress conditions and accompanies photoinhibition of photosystem II. Plant Physiol 100:1554–1561CrossRefGoogle Scholar
  60. Fidalgo F, Azenha M, Silva AF, de Sousa A, Santiago A, Ferraz P, Teixeira J (2013) Copper-induced stress in Solanum nigrum L. and antioxidant defense system responses. Food Energy Sec 2:70–80CrossRefGoogle Scholar
  61. Finatto T, de Oliveira AC, Chaparro C, da Maia LC, Farias DR, Woyann LG, Mistura CC, et al. (2015) Abiotic stress and genome dynamics: specific genes and transposable elements response to iron excess in rice. Rice 8:13. doi: 10.1186/s12284-015-0045-6 CrossRefGoogle Scholar
  62. Fourcroy P, Vansuyt G, Kushnir S, Inzé D, Briat JF (2004) Iron-regulated expression of a cytosolic ascorbate peroxidase encoded by the APX1 gene in Arabidopsis seedlings. Plant Physiol 134:605–613CrossRefGoogle Scholar
  63. Frugoli JA, Zhong HH, Nuccio ML, McCourt P, McPeek MA, Thomas TL, McClung CR (1996) Catalase is encoded by a multigene family in Arabidopsis thaliana L. Heynh. Plant Physiol 112:327–336CrossRefGoogle Scholar
  64. Gadea J, Conejero V, Vera P (1999) Developmental regulation of a cytosolic ascorbate peroxidase gene from tomato plants. Mol Gen Genet 262:212–219CrossRefGoogle Scholar
  65. Gajewska E, Sklodowska M (2008) Differential biochemical responses of wheat shoots and roots to nickel stress: antioxidative reactions and proline accumulation. Plant Growth Regul 54:179–188CrossRefGoogle Scholar
  66. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101CrossRefGoogle Scholar
  67. Ghaderi N, Normohammadi S, Javadi T (2015) Morpho-physiological responses of strawberry (Fragaria × ananassa) to exogenous salicylic acid application under drought stress. J Agric Sci Technol 17:167–178Google Scholar
  68. Gichner T, Patkova Z, Szakova J, Demnerova K (2004) Cadmium induces DNA damages in tobacco roots, but no DNA damage, somatic mutations or homologous recombinations in tobacco leaves. Mutat Res Genet Toxicol Environ Mutagen 559:49–57CrossRefGoogle Scholar
  69. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefGoogle Scholar
  70. Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, et al. (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212CrossRefGoogle Scholar
  71. Gomes-Júnior RA, Moldes CA, Delite FS, Pompeu GB, Gratão PL, et al. (2006) Antioxidant metabolism of coffee cell suspension cultures in response to cadmium. Chemosphere 65:1330–1337CrossRefGoogle Scholar
  72. Gondim FA, Miranda RD, Gomes-Filho E, Prisco JT (2013) Enhanced salt tolerance in maize plants induced by H2O2 leaf spraying is associated with improved gas exchange rather than with non-enzymatic antioxidant system. Theor Exp Plant Physiol 25(4):251-60Google Scholar
  73. Gong H, Zhu X, Chen K, Wang S, Zhang C (2005) Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci 169:313–321CrossRefGoogle Scholar
  74. Groden D, Beck E (1979) H2O2 destruction by ascorbate-dependent systems from chloroplasts. Biochim Biophys Acta 546:426–435CrossRefGoogle Scholar
  75. Guan L, Scandalios JG (1993) Characterization of the catalase antioxidant defense gene Cat1 of maize and its developmentally regulated expression in transgenic tobacco. Plant J 3:527–536CrossRefGoogle Scholar
  76. Guan L, Scandalios JG (1995) Developmentally related response of maize catalase genes to salicylic acid. Proc Natl Acad Sci U S A 92:5930–5934CrossRefGoogle Scholar
  77. Guan L, Scandalios JG (1996) Molecular evolution of maize catalases and their relationship to other eukaryotic and prokaryotic catalases. J Mol Evol 42:570–579CrossRefGoogle Scholar
  78. Guan ZQ, Chai TY, Zhang YX, Xu J, Wei W (2009) Enhancement of Cd tolerance in transgenic tobacco plants overexpressing a Cd-induced catalase cDNA. Chemosphere 76:623–630CrossRefGoogle Scholar
  79. Guiltinan MJ, Marcotte WR, Quatrano RS (1990) A plant leucine zipper protein recognizes an abscisic acid response element. Science 250:267–270CrossRefGoogle Scholar
  80. Guo Q, Meng L, Mao PC, Jia YQ, Shi YJ (2013) Role of exogenous salicylic acid in alleviating cadmium induced toxicity in Kentucky bluegrass. Biochem Syst Ecol 50:269–276CrossRefGoogle Scholar
  81. 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 143:1758–1776Google Scholar
  82. Hasanuzzaman M, Fujita M (2013a) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22:584–596CrossRefGoogle Scholar
  83. Hasanuzzaman M, Hossain MA, Fujita M (2011a) Selenium-induced up-regulation of the antioxidant defense and methylglyoxal detoxification system reduces salinity-induced damage in rapeseed seedlings. Biol Trace Elem Res 143:1704–1721CrossRefGoogle Scholar
  84. Hasanuzzaman M, Hossain MA, Fujita M (2011b) Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol Rep 5:353–365CrossRefGoogle Scholar
  85. Hasanuzzaman M, Hossain MA, JA T d S, Fujita M (2012a) 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. 261–316CrossRefGoogle Scholar
  86. Hasanuzzaman M, Nahar K, Alam MM, Fujita M (2012b) Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum L.) seedlings by modulating the antioxidant defense and glyoxalase system. Aust J Crop Sci 6:1314–1323Google Scholar
  87. Hasanuzzaman M, Alam MM, Nahar K, Mahmud JA, Ahamed KU, Fujita M (2014a) Exogenous salicylic acid alleviates salt stress-induced oxidative damage in Brassica napus by enhancing the antioxidant defense and glyoxalase systems. Aus J Crop Sci 8:631–639Google Scholar
  88. Hasanuzzaman M, Alam MM, Rahman A, Hasanuzzaman M, Nahar K, Fujita M (2014b) Exogenous poline and glycine betaine mediated upregulation of antioxidant defense and glyoxalase systems provides better protection against salt-induced oxidative stress in two rice (Oryza sativa L.) varieties. BioMed Res Intl. doi: 10.1155/2014/757219S Google Scholar
  89. Hasanuzzaman M, Nahar K, MM A, Fujita M (2014c) Modulation of antioxidant machinery and the methylglyoxal detoxification system in selenium-supplemented Brassica napus seedlings confers tolerance to high temperature. Biol Trace Elem Res 161:297–307CrossRefGoogle Scholar
  90. Havir EA, McHale NA (1989) Enhanced-peroxidatic activity in specific catalase isozymes of tobacco, barley, and maize. Plant Physiol 91(3):812–815CrossRefGoogle Scholar
  91. Hayat S, Ali B, Hasan SA, Ahmad A (2007) Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. Environ Exp Bot 60:33–41CrossRefGoogle Scholar
  92. Heazlewood JL, Tonti-Filipinni JS, Gout AM, Day DA, Whelan J, Millar AH (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16:241–256CrossRefGoogle Scholar
  93. Heidenreich B, Mayer K, Sandermann H Jr, Ernst D (2001) Mercury-induced genes in Arabidopsis thaliana: identification of induced genes upon long-term mercuric ion exposure. Plant Cell Environ 24:1227–1234CrossRefGoogle Scholar
  94. Hernandez J, Jimenez A, Millineaus P, Sevilla F (2000) Tolerance to pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defenses. Plant Cell Environ 23:853–862CrossRefGoogle Scholar
  95. Hochman A, Goldberg I (1991) Purification and characterization of a catalase-peroxidase and a typical catalase from the bacterium Klebsiella pneumonia. Biochim Biophys Acta 7107:299–307CrossRefGoogle Scholar
  96. Hoque MA, Banu MNA, Okuma E, Amako K, Nakamura Y, Shimoishi Y, Murata Y (2006) Exogenous proline and glycinebetaine increase NaCl-induced ascorbate–glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells. J Plant Physiol 164:1457–1468CrossRefGoogle Scholar
  97. 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. 81–147Google Scholar
  98. 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 16:259–272CrossRefGoogle Scholar
  99. Hossain MA, Piyatida P, da Silva JA, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot. doi: 10.1155/2012/872875
  100. Hossain MA, Bhattacharjee S, Armin S, Qian P, Xin W, Li H, et al. (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420Google Scholar
  101. Houseman ALP, Doan PE, Goodin DB, Hoffman BM (1993) Comprehensive explanation of the anomalous EPR spectra of wild-type and mutant cytochrome- c peroxidase compound-ES. Biochemistry 32:4430–4443CrossRefGoogle Scholar
  102. Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238CrossRefGoogle Scholar
  103. Hu X, Jiang M, Zhang A, Lu J (2005) Abscisic acid induced apoplastic H2O2 accumulation upregulates the activities of chloroplastic and cytosolic antioxidant enzymes in maize leaves. Planta 223:57–68CrossRefGoogle Scholar
  104. Hu YQ, Liu S, Yuan HM, Li J, Yan DW, Zhang JF, Lu YT (2010) Functional comparison of catalase genes in the elimination of photorespiratory H2O2 using promoter- and 3′-untranslated region exchange experiments in the Arabidopsis cat2 photorespiratory mutant. Plant Cell Environ 33:1656–1670CrossRefGoogle Scholar
  105. Huang GY, Wang YS, Sun CC, Dong JD, Sun ZX (2010) The effect of multiple heavy metals on ascorbate, glutathione and related enzymes in two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Oceanol Hydrobiol Stud 39:11–25CrossRefGoogle Scholar
  106. Ibrahim MM, Bafeel SO (2009) Alteration of gene expression, superoxide anion radical and lipid peroxidation induced by lead toxicity in leaves of Lepidium sativum. J Anim Plant Sci 4:281–288Google Scholar
  107. Ishikawa T, Shigeoka S (2008) Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem 72:1143–1154CrossRefGoogle Scholar
  108. Ishikawa T, Sakai K, Yoshimura K, Takeda T, Shigeoka S (1996) cDNAs encoding spinach stromal thylakoid bound ascorbate peroxidase, differing in the presence or absence of their 39-coding regions. FEBS Lett 384:289–293CrossRefGoogle Scholar
  109. Ishikawa T, Yoshimura K, Tamoi M, Takeda T, Shigeoka S (1997) Alternative mRNA splicing of 39-terminal exons generates ascorbate peroxidase isoenzymes in spinach (Spinacia oleacea) chloroplast. Biochem J 328:795–800CrossRefGoogle Scholar
  110. 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 39:23–34CrossRefGoogle Scholar
  111. 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 186:1520–1526CrossRefGoogle Scholar
  112. Iwamoto M, Maekawa M, Saito A, Higo H, Higo K (1998) Evolutionary relationship of plant catalase genes inferred from exon-intron structures, isozyme divergence after the separation of monocots and dicots. Theor Appl Genet 97:9–19CrossRefGoogle Scholar
  113. Iwamoto M, Higo H, Higo K (2000) Differential diurnal expression of rice catalase genes, the 5′-flanking region of CatA is not sufficient for circadian control. Plant Sci 151:39–46CrossRefGoogle Scholar
  114. Iwase T, Tajima A, Sugimoto S, Okuda KI, Hironaka I, et al. (2013) A simple assay for measuring catalase activity: a visual approach. Sci Report 3Google Scholar
  115. Jespersen HM, KjaersgardIvh OL, Welinder KG (1997) From sequence analysis of three novel APXs from Arabidopsis thaliana to structure, function and evolution of seven types of APX. Biochem J 326:305–310CrossRefGoogle Scholar
  116. Jimenez A, Hernandez 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 114:275–284Google Scholar
  117. Kabir MH, Wang MH (2011) Functional studies on two catalase genes from tomato (Solanum lycopersicum L.). J Hortic Sci Biotechnol 86:84–90CrossRefGoogle Scholar
  118. Karyotou K, Donaldson RP (2005) Ascorbate peroxidase, a scavenger of hydrogen peroxide in glyoxysomal membranes. Arch Biochem Biophys 434:248–257CrossRefGoogle Scholar
  119. Kavitha K, Venkataraman G, Parida A (2008) An oxidative and salinity stress induced peroxisomal ascorbate peroxidase from Avicennia marina: molecular and functional characterization. Plant Physiol Biochem 46:794–804CrossRefGoogle Scholar
  120. Kaya A, Yigi E (2014) The physiological and biochemical effects of salicylic acid on sunflowers (Helianthus annuus) exposed to flurochloridone. Ecotoxicol Environ Saf 106:232–238CrossRefGoogle Scholar
  121. Kelly GJ, Latzko E (1979) Soluble ascorbate peroxidase, detection in plants and use in vitamin C estimation. Naturwissenschaften 66:617–619Google Scholar
  122. 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 193:435–444CrossRefGoogle Scholar
  123. Khatun S, Ali MB, Hahn EJ, Paek KY (2008) Copper toxicity in Withania somnifera: growth and antioxidant enzymes responses of in vitro grown plants. Environ Exp Bot 64:279–285CrossRefGoogle Scholar
  124. Kim KH, Kim YN, Lim GH, Lee MN, Jung YH (2011) Expression of catalase (CAT) and ascorbate peroxidase (APX) in MuSI transgenic tobacco under cadmium stress. Korean J Soil Sci Fert 44:53–57CrossRefGoogle Scholar
  125. Kirkman HN, Gaetani GF (1984) Catalase, a tetrameric enzyme with four tightly bound molecules of NADPH. Proc Natl Acad Sci U S A 14:4343–4347CrossRefGoogle Scholar
  126. König J, Baier M, Horling F, Kahmann U, Harris G, et al. (2002) The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. Proc Natl Acad Sci U S A 99:5738–5743CrossRefGoogle Scholar
  127. Kovacsa FA, Sarathb G, Woodwortha K, Twiggc P, Tobiasd CM (2013) Abolishing activity against ascorbate in a cytosolic ascorbate peroxidase from switch grass. Phytochemistry 94:45–52CrossRefGoogle Scholar
  128. 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 165:920–931CrossRefGoogle Scholar
  129. Kumutha D, Ezhilmathi K, Sairam RK, Srivastava GC, Deshmukh PS, Meena RC (2009) Waterlogging induced oxidative stress and antioxidant activity in pigeonpea genotype. Biol Plant 53:75–84CrossRefGoogle Scholar
  130. Kwon SI, An CS (2001) Molecular cloning, characterization and expression analysis of a catalase cDNA from hot pepper (Capsicum annuum L.). Plant Sci 160:961–969CrossRefGoogle Scholar
  131. Lad L, Mewiers M, Lloyd Raven E (2002) Substrate binding and catalytic mechanism in ascorbate peroxidase, evidence for two ascorbate binding sites. Biochemistry 41:13774–13781CrossRefGoogle Scholar
  132. Lazzarotto F, Teixeira FK, Rosa SB, Dunand C, Fernandes CL, de Vasconcelos FA, Silveira JA, Verli H, Margis R, Margis-Pinheiro M (2011) Ascorbate peroxidase-related (APx-R) is a new heme-containing protein functionally associated with ascorbate peroxidase but evolutionarily divergent. New Phytol 91:234–250CrossRefGoogle Scholar
  133. Lee MY, Shin HW (2003) Cadmium-induced changes in antioxidant enzymes from marine alga Nannochloropsis oculata. J Appl Phycol 15:13–19CrossRefGoogle Scholar
  134. Lee SH, Ahsan N, Lee KW, Kim DH, Lee DG, et al. (2007) Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol 164:1626–1638CrossRefGoogle Scholar
  135. Li YJ, Hai RL, Du XH, Jiang XN, Lu H (2009) Over-expression of a Populus peroxisomal ascorbate peroxidase (PpAPX) gene in tobacco plants enhances stress tolerance. Plant Breed 128:404–410CrossRefGoogle Scholar
  136. Li X, Ma H, Jia P, Wang J, Jia L, Zhang T, et al. (2012) Responses of seedling growth and antioxidant activity to excess iron and copper in Triticum aestivum L. Ecotoxicol Environ Saf 86:47–53CrossRefGoogle Scholar
  137. Lin KH, Pu SF (2010) Tissue- and genotype-specific ascorbate peroxidase expression in sweet potato in response to salt stress. Biol Plant 54:664–670CrossRefGoogle Scholar
  138. Lin KH, Lo HF, Lin CH, Chan MS (2007) Cloning and expression analysis of ascorbate peroxidase gene from eggplant under flooding stress. Bo Stud 48:25–34Google Scholar
  139. Lisenbee CS, Heinze M, Trelease RN (2003) Peroxisomal APX resides within a subdomain of rough endoplasmic reticulum in wild-type Arabidopsis cells. Plant Physiol 132:870–882CrossRefGoogle Scholar
  140. Liu Y, Yaoa Y, Hua X, Xinga S, Xua L (2015) Cloning and allelic variation of two novel catalase genes (SoCAT-1 and SsCAT-1) in Saccharum officinarum L. and Saccharum spontaneum L. Biotechnol Biotechnol Equip. doi: 10.1080/13102818.2015.1018839 Google Scholar
  141. Loew O (1901) Catalase, new enzyme of general occurrence, with special reference to the tobacco plant. US Depart Agric Rep 68:47Google Scholar
  142. Lombardi L, Sebastiani L (2005) Copper toxicity in Prunus cerasifera: growth and antioxidant enzymes responses of in vitro grown plants. Plant Sci 168:797–802CrossRefGoogle Scholar
  143. Lomonte C, Sgherri C, Baker AJM, Kolev SD, Navari-Izzo F (2010) Antioxidative response of Atriplex codonocarpa to mercury. Environ Exp Bot 69:9–16CrossRefGoogle Scholar
  144. Lopez-Huertas E, del Río LA (2014) Characterization of antioxidant enzymes and peroxisomes of olive (Olea europaea L) fruits. J Plant Physiol 171:1463–1471CrossRefGoogle Scholar
  145. Lopez-Huertas E, Corpas FJ, Salio LM, del Río LA (1999) Characterization of membrane polypeptides from pea leaf peroxisomes involved in superoxide radical generation. Biochem J 337:531–536CrossRefGoogle Scholar
  146. Luo H, Li H, Zhang X, Fu J (2011) Antioxidant responses and gene expression in perennial ryegrass (Lolium perenne L.) under cadmium stress. Ecotoxicology 20:770–778CrossRefGoogle Scholar
  147. Lyubenova L, Schröder P (2011) Plants for waste water treatment effects of heavy metals on the detoxification system of Typha latifolia. Bioresour Technol 102:996–1004CrossRefGoogle Scholar
  148. Ma QQ, Wang W, Li YH, Li DQ, Zou Q (2006) Alleviation of photoinhibition in drought-stressed wheat (Triticum aestivum) by foliar-applied glycinebetaine. J Plant Physiol 163:165–175CrossRefGoogle Scholar
  149. MacDonald IK, Badyal SK, Ghamsari L, Moody PCE, Raven EL (2006) Interaction of ascorbate peroxidase with substrates - a mechanistic and structural analysis. Biochemistry 45:7808–7817CrossRefGoogle Scholar
  150. Madhusudhan R, Ishikawa T, Sawa Y, Shigeoka S, Shibata H (2003) Characterization of an ascorbate peroxidase in plastids of tobacco BY–2 cells. Physiol Plant 117:550–557CrossRefGoogle Scholar
  151. Manai J, Kalai T, Gouia H, Corpas FJ (2014) Exogenous nitric oxide (NO) ameliorates salinity-induced oxidative stress in tomato (Solanum lycopersicum) plants. J Soil Sci Plant Nutr 14:433–446Google Scholar
  152. Mandelman D, Jamal J, Poulos TL (1998a) Identification of two electron-transfer sites in ascorbate peroxidase using chemical modification, enzyme kinetics crystallography. Biochemistry 37:17610–17617CrossRefGoogle Scholar
  153. Mandelman D, Schwarz FP, Li H, Poulos TL (1998b) The role of quaternary interactions on the stability activity of ascorbate peroxidase. Protein Sci 7:2089–2098CrossRefGoogle Scholar
  154. Mano S, Yamaguchi K, Hayashi M, Nishimura M (1997) Stromal thylakoid-bound ascorbate peroxidases are produced by alternative splicing in pumpkin. FEBS Lett 413:21–26CrossRefGoogle Scholar
  155. Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178Google Scholar
  156. Mhamdi A, Queval G, Chaouch S, Vanderauwera S, et al. (2010) Catalase function in plants, a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot 61:4197–4220CrossRefGoogle Scholar
  157. Minglin L, Yuxiu Z, Tuanyao C (2005) Identification of genes up-regulated in response to Cd exposure in Brassica juncea L. Gene 363:151–158CrossRefGoogle Scholar
  158. Mitsuda H, Yasumatsu K (1955) Studies on plant catalase. Bull Agric Chem Soc Jpn 19:208–213CrossRefGoogle Scholar
  159. Mittler R, Zilinskas BA (1991a) Purification and characterization of pea cytosolic ascorbate peroxidase. Plant Physiol 97:962–968CrossRefGoogle Scholar
  160. Mittler R, Zilinskas BA (1991b) Molecular cloning and nucleotide sequence analysis of a cDNA encoding pea cytosolic ascorbate peroxidase. FEBS Lett 289:257–259CrossRefGoogle Scholar
  161. Mittler R, Zilinskas BA (1992) Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase. J Biol Chem 267:21802–21807Google Scholar
  162. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498CrossRefGoogle Scholar
  163. Mittova V, Tal M, Volokita M, Guy M (2003a) Upregulation 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 26:845–856CrossRefGoogle Scholar
  164. Mittova V, Guy M, Tal M, Volokita M (2004a) Salinity upregulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 55:1105–1113CrossRefGoogle Scholar
  165. Mittova V, Theodoulou FL, Kiddle G, Volokita M, et al. (2004b) Comparison of mitochondrial APX in the cultivated tomato, Lycopersicon esculentum, its wild, salt-tolerant relative, L. pennellii– role for matrix isoforms in protection against oxidative damage. Plant Cell Environ 27:237–250CrossRefGoogle Scholar
  166. Miyake C, Asada K (1996) Inactivation of mechanism of ascorbate peroxidase at low concentrations of ascorbate, hydrogen peroxide decomposes compound I of ascorbate peroxidase. Plant Cell Physiol 37:423–430CrossRefGoogle Scholar
  167. Miyake C, Cao WH, Asada K (1993) Purification and molecular properties of thylakoid-bound ascorbate peroxidase from spinach chloroplasts. Plant Cell Physiol 343:881–889Google Scholar
  168. 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 164:601–610CrossRefGoogle Scholar
  169. Mondal P, Ray M, Sahu S, Sabat SC (2008a) Co-expression of GroEL/ES enhances the expression of plant catalase in bacterial cytosol. Protein Pept Lett 15(10):1075–1078CrossRefGoogle Scholar
  170. Mondal P, Ray M, Kar M, Sabat SC (2008b) Molecular identification and properties of a light-insensitive rice catalase-B expressed in E. coli. Biotechnol Lett 30(3):563–856CrossRefGoogle Scholar
  171. Mora ML, Rosas A, Ribera A, Rengel Z (2009) Differential tolerance to Mn toxicity in perennial ryegrass genotypes: involvement of antioxidative enzymes and root exudation of carboxylates. Plant Soil 320:79–89CrossRefGoogle Scholar
  172. Mullen RT, Trelease RN (2000) The sorting signals for peroxisomal membrane-bound ascorbate peroxidase are within its C-terminal tail. J Biol Chem 275:16337–16344CrossRefGoogle Scholar
  173. Mullen RT, Lisenbee CS, Flynn CR, Trelease RN (2001) Stable transient expression of chimeric peroxisomal membrane proteins induces an independent “ziering” of peroxisomes an endoplasmic reticulum subdomain. Planta 213:849–863CrossRefGoogle Scholar
  174. Mutsada M, Ishikawa T, Takeda T, Shigeoka S (1996) The catalase-peroxidase of Synechococcus PCC 7942, purification, nucleotide sequence analysis and expression in Escherichia coli. Biochem J 316:251–257CrossRefGoogle Scholar
  175. Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015a) Regulatory roles of exogenous glutathione in conferring salt tolerance in mung bean (Vigna radiata L.): implication of antioxidant defense and methylglyoxal detoxification systems. Biol Plant. doi: 10.1007/s10535-015-0542-x Google Scholar
  176. Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015b) Glutathione-induced drought stress tolerance in mung bean: coordinated roles of the antioxidant defense and methylglyoxal detoxification systems. AoB Plants. doi: 10.1093/aobpla/plv069 Google Scholar
  177. Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015c) Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata L.) by modulating antioxidant defense and methylglyoxal detoxification system. Environ Exp Bot 112:44–54CrossRefGoogle Scholar
  178. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  179. Neill SJ, Desikan R, Clarke A (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53:1237–1242CrossRefGoogle Scholar
  180. Neto ADA, Prisco JT, Eneas-Filho J, Medeiros JVR, Gomes-Filho E (2005) Hydrogen peroxide pre-treatment induces salt stress acclimation in maize plants. J Plant Physiol 162:1114–1122CrossRefGoogle Scholar
  181. Nie Q, Gao GL, Fan QJ, Qiao G, Wen XP, Liu T, Peng ZJ, Cai YQ (2015) Isolation and characterization of a catalase gene “HuCAT3” from pitaya (Hylocereus undatus) and its expression under abiotic stress. Gene. doi: 10.1016/j.gene.2015.03.007 Google Scholar
  182. Nishikawa F, Kato M, Hyodo H, Ikoma Y, Sugiura M, Yano M (2003) Ascorbate metabolism in harvested broccoli. J Exp Bot 54:2439–2448CrossRefGoogle Scholar
  183. Nito K, Yamaguchi K, Kondo M, Hayashi M, Nishimura M (2001) Pumpkin peroxisomalascorbate peroxidase is localized on peroxisomal membranes and unknown membranous structures. Plant Cell Physiol 42:20–27CrossRefGoogle Scholar
  184. Noctor G, Foyer CH (1998) Ascorbate and glutathione—keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279CrossRefGoogle Scholar
  185. Noctor G, Mhamdi A, Chaouch S, Han YI, Neukermans J, Marquez-Garcia B, et al. (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484CrossRefGoogle Scholar
  186. Okuda A, Imagawa M, Maeda Y, Sakai M, Muramatsu M (1989) Structural and functional analysis of an enhancer GPE I having a phorbol 12-0-tetradecanoate 13-acetate responsive element-like sequence found in the rat glutathione transferase P gene. J Biol Chem Mol Biol 264:16919–16926Google Scholar
  187. Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191CrossRefGoogle Scholar
  188. Oshino N, Jamieson D, Sugano T, Chance B (1975) Optical measurement of the catalase-hydrogen peroxide intermediate compound I in the level of anaesthetized rats and its implication to H2O2 production in vivo. Biochem J 146:67–77CrossRefGoogle Scholar
  189. Panchuk I, Volkov R, Schöffl F (2002) Heat stress and heat shock transcription factor-dependent expression and activity of APX in Arabidopsis. Plant Physiol 129:838–853CrossRefGoogle Scholar
  190. Panda SK, Matsumoto H (2010) Changes in antioxidant gene expression and induction of oxidative stress in pea (Pisum sativum L.) under Al stress. Biometals 23:753–762CrossRefGoogle Scholar
  191. Park SY, Ryu SH, Jang IC, Kwon SY, Kim JG, Kwak SS (2004) Molecular cloning of a cytosolic ascorbate peroxidase cDNA from cell cultures of sweet potato and its expression in response to stress. Mol Gen Genomics 271:339–346CrossRefGoogle Scholar
  192. Pastori GM, Trippi VS (1992) Oxidative stress induces high rate of glutathione reductase synthesis in a drought resistant maize strain. Plant Cell Physiol 33:957–961Google Scholar
  193. Patterson WR, Poulos TL, Goodin DB (1995) Identification of a porphyrin pi cation radical in ascorbate peroxidase compound I. Biochemistry 34:4342–4345CrossRefGoogle Scholar
  194. 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 49:429–438CrossRefGoogle Scholar
  195. Pereira CS, Da Costa DS, Teixeira J, Pereira S (2005) Organ-specific distribution and subcellular localization of APXisoenzymes in potato Solanumtuberosum L. plants. Protoplasma 226:223–230CrossRefGoogle Scholar
  196. Polidoros AN, Scandalios JG (1997) Response of the maize catalases to light. Free Radic Biol Med 23:497–504CrossRefGoogle Scholar
  197. 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 72:596–602CrossRefGoogle Scholar
  198. Proietti P, Nasini L, Buono DD, D’Amato R, Tedeschini E, Businelli D (2013) Selenium protects olive (Olea europaea L.) from drought stress. Sci Hortic 164:165–171CrossRefGoogle Scholar
  199. Purev M, Kim YJ, Kim MK, Pulla RK, Yang DC (2010) Isolation of a novel catalase (Cat1) gene from Panax ginseng and analysis of the response of this gene to various stresses. Plant Physiol Biochem 48:451–460CrossRefGoogle Scholar
  200. Qiu ZB, Guo JL, Zhu AJ, Zhang L, Zhang MM (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicol Environ Saf 104:202–208CrossRefGoogle Scholar
  201. Quinet M, Vromman D, Clippe A, Bertin P, Lequeux H, Dufey I, Lutts S, Lefèvre I (2012) Combined transcriptomic and physiological approaches reveal strong differences between short- and long-term response of rice (Oryza sativa) to iron toxicity. Plant Cell Environ 35:1837–1859CrossRefGoogle Scholar
  202. Ray M, Mishra P, Das P, Sabat SC (2012) Expression and purification of soluble bio-active rice plant catalase-A from recombinant Escherichia coli. J Biotechnol 157(1):12–19CrossRefGoogle Scholar
  203. Redinbaugh MG, Sabre M, Scandalios JG (1990) Expression of the maize Cat3 catalase gene in under the influence of a circadian rhythm. Proc Natl Acad Sci U S A 87:6853–6857CrossRefGoogle Scholar
  204. Regelsberger G, Jakopitsch C, Furtmüller PG, Rueker F, Switala J, Loewen PC, Obinger C (2001) The role of distal tryptophan in the bifunctional activity of catalase-peroxidases. Biochem Soc Trans 29:99–105CrossRefGoogle Scholar
  205. Regelsberger G, Jakopitsch C, Plasser L, Schwaiger H, Furtmüller PG, Peschek GA, Zámocky M, Obinger C (2002) Occurrence and biochemistry of hydrogen peroxidase in oxygenic phototrophic prokaryotes (cyanobacteria). Plant Physiol Biochem 40:479–490CrossRefGoogle Scholar
  206. Rellán-Álvarez R, Ortega-Villasante C, Álvarez-Fernández A, del Campo FF, Hernández LE (2006) Stress responses of Zea mays to cadmium and mercury. Plant Soil 279:41–50CrossRefGoogle Scholar
  207. Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116:409–418CrossRefGoogle Scholar
  208. Rizhsky L, Davletova S, Liang H, Mittler R (2004) The zinc-finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279:11736–11743CrossRefGoogle Scholar
  209. Romero-Puertas MC, McCarthy I, Sandalio LM, Palma JM, Corpas FJ, Gómez M, Del Río LA (1999) Cadmium toxicity and oxidative metabolism of pea leaf peroxisomes. Free Radic Res 31:S25–S32CrossRefGoogle Scholar
  210. Romero-Puertas MC, Palma JM, Gómez M, del Río LA, Sandalio LM (2002) Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25:677–686CrossRefGoogle Scholar
  211. Rorth M, Jensen PK (1967) Determination of catalase activity by means of the Clark oxygen electrode. Biochim Biophys Acta 139:171–173CrossRefGoogle Scholar
  212. Rosa SB, Caverzan A, Teixeira FK, Lazzarotto F, Silveira JA, Ferreira-Silva SL, et al. (2010) Cytosolic APx knockdown indicates an ambiguous redox responses in rice. Phytochemistry 71:548–558CrossRefGoogle Scholar
  213. Roupakias DG, McMillin DE, Scandalios JG (1980) Chromosomal location of the catalase structural genes in Zea mays, using B-A translocations. Theor Appl Genet 58:211–218Google Scholar
  214. Saidi I, Nawel N, Djebali W (2014) Role of selenium in preventing manganese toxicity in sunflower (Helianthus annuus) seedling. South Afr J Bot 94:88–94CrossRefGoogle Scholar
  215. Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Río RA (2001) Cadmium-induced changes in growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126Google Scholar
  216. Sato Y, Murakami T, Funatsuki H, Matsuba S, Saruyama H, Tanida M (2001) Heat shock-mediated APX gene expression and protection against chilling injury in rice seedlings. J Exp Bot 52:145–151CrossRefGoogle Scholar
  217. Scandalios JG (1968) Genetic control of multiple molecular forms of catalase in maize. Ann N Y Acad Sci 151:274–293CrossRefGoogle Scholar
  218. Scandalios JG (1990) Response of plant antioxidant defense genes to environmental stress. Adv Genet 28:1–41Google Scholar
  219. Scandalios JG, Guan L, Polidoros AN (1997) Catalases in plants, gene structure, properties, regulation and expression. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defences cold spring. Harbor Laboratory Pres, NY, pp. 343–406Google Scholar
  220. Schepartz AI (1974) Method for the determination of catalase activity in tobacco. Tobacco Sci 18:52–54Google Scholar
  221. 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 75:887–898CrossRefGoogle Scholar
  222. Schützendübel A, Nikolova P, Rudolf C, Polle A (2002) Cadmium and H2O2-induced oxidative stress in Populus canescens roots. Plant Physiol Biochem 40:577–584CrossRefGoogle Scholar
  223. Sekhar PN, Kishor PB, Reddy LA, Mondal P, Dash AK, et al. (2006) In silico modeling and hydrogen peroxide binding study of rice catalase. In Silico Biol 6(5):435–447Google Scholar
  224. Shahbaz M, Ashraf M (2013) Improving salinity tolerance in cereals. Crit Rev Plant Sci 32:237–249CrossRefGoogle Scholar
  225. Sharma P, Dubey RS (2004) APX from rice seedlings, properties of enzyme isoforms, effects of stresses and protective roles of osmolytes. Plant Sci 167:541–550CrossRefGoogle Scholar
  226. Sharma P, Dubey RS (2005) Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regul 46:209–221CrossRefGoogle Scholar
  227. 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 26:2027–2038CrossRefGoogle Scholar
  228. 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
  229. Sharma I, Ching E, Saini S, Bhardwaj R, Pati PK (2013) Exogenous application of brassinosteroid offers tolerance to salinity by altering stress responses in rice variety Pusa basmati-1. Plant Physiol Biochem 69:17–26CrossRefGoogle Scholar
  230. Sharp KH, Mewies M, Moody PCE, Raven EL (2003) Crystal structure of the ascorbate peroxidase–ascorbate complex. Nat Struct Biol 10:303–307CrossRefGoogle Scholar
  231. Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, et al. (2002) Regulation and function of APX isoenzymes. J Exp Bot 53:1305–1319CrossRefGoogle Scholar
  232. Shikanai T, Takeda T, Yamauchi H, Sano S, Tomizawa KI, et al. (1998) Inhibition of ascorbate peroxidase under oxidative stress in tobacco having bacterial catalase in chloroplasts. FEBS Lett 428:47–51CrossRefGoogle Scholar
  233. Shugaev AG, Lashtabega DA, Shugaeva NA, Vyskrebentseva EI (2011) Activities of antioxidant enzymes in mitochondria of growing and dormant sugar beet roots. Russ J Plant Physiol 58:387–393CrossRefGoogle Scholar
  234. Simova-Stoilova L, Vaseva I, Grigorova B, Demirevska K, Feller U (2010) Proteolytic activity and cysteine protease expression in wheat leaves under severe soil drought and recovery. Plant Physiol Biochem 48:200–206CrossRefGoogle Scholar
  235. 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 3:25–32CrossRefGoogle Scholar
  236. Singh N, Mishra A, Jha B (2014a) Ectopic over-expression of peroxisomal ascorbate peroxidase (SbpAPX) gene confers salt stress tolerance in transgenic peanut (Arachis hypogaea). Gene 547:119–125CrossRefGoogle Scholar
  237. Singh N, Mishra A, Jha B (2014b) Over-expression of the peroxisomal ascorbate peroxidase (SbpAPX) gene cloned from halophyte Salicornia brachiate confers salt and drought stress tolerance in transgenic tobacco. Mar Biotechnol 16:321–332CrossRefGoogle Scholar
  238. Sinha AK (1972) Colorimetric assay of catalase. Anal Biochem 47:389–394CrossRefGoogle Scholar
  239. Sobrino-Plata J, Ortega-Villasante C, Flores-Cáceres ML, Escobar C, Del Campo FF, Hernández LE (2009) Differential alterations of antioxidant defenses as bioindicators of mercury and cadmium toxicity in alfalfa. Chemosphere 77:946–954CrossRefGoogle Scholar
  240. Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci 16(6):13561–13578CrossRefGoogle Scholar
  241. Solanki R, Poonam A (2011) Zinc and copper induced changes in physiological characteristics of Vigna mungo (L.). J Environ Biol 32:747–751Google Scholar
  242. Sooch BS, Kauldhar BS, Puri M (2014) Recent insights into microbial catalases: isolation, production and purification. Biotechnol Adv 32(8):1429–1447CrossRefGoogle Scholar
  243. Sørensen PH, Mortensen KK (2005) Soluble expression of recombinant proteins in the cytoplasm of Escherichia coli. Microb Cell Factories 4(2005):1CrossRefGoogle Scholar
  244. Sreedevi S, Krishnan PN, Pushpangadan (2008) Cadmium induced oxidative stress and antioxidant responses in roots of black gram [Vigna mungo (L.) Hepper]. Ind J Plant Physiol 13:1–7Google Scholar
  245. Srivastava AK, Bhargava P, Rai LC (2005) Salinity and copper-induced oxidative damage and changes in antioxidative defense system of Anabaena doliolum. World J Microbiol Biotechnol 22:1291–1298CrossRefGoogle Scholar
  246. Stansell MJ, Deutsch HF (1965) Physicochemical studies of crystalline human erythrocuprein. J Biol Chem 240:4299–4305Google Scholar
  247. Storozhenko S, Pauw PD, Montagu MV, Inzé D, Kushnir S (1998) The heat-shock element is a functional component of the Arabidopsis APX1 gene promoter. Plant Physiol 118:1005–1014CrossRefGoogle Scholar
  248. Su Y, Guo J, Ling H, Chen S, Wang S, Xu L, Allan AC, Que Y (2014) Isolation of a novel peroxisomal catalase gene from sugarcane, which is responsive to biotic and abiotic stresses. PLoS One. doi: 10.1371/journal.pone.0084426 Google Scholar
  249. Sumner JB, Dounce AL (1937) Crystalline catalase. J Biol Chem 121:417–424Google Scholar
  250. Sun WH, Duan M, Li F, Shu DF, Yang S, Meng QW (2010) Overexpression of tomato tAPX gene in tobacco improves tolerance to high or low temperature stress. Biol Plant 54:614–620CrossRefGoogle Scholar
  251. Switala J, Loewen PC (2002) Diversity of properties among catalases. Arch Biochem Biophys 401:145–154CrossRefGoogle Scholar
  252. Teixeira FK, Menezes-Benavente L, Margis R, Margis-Pinheiro M (2004) Analysis of the molecular evolutionary history of the ascorbate peroxidase gene family, inferences from the rice genome. J Mol Evol 59:761–770CrossRefGoogle Scholar
  253. Teixeira FK, Menezes-Benavente L, Galvão VC, Margis-Pinheiro M (2005) Multigene families encode the major enzymes of antioxidant metabolism in Eucalyptus grandis L. Genet Mol Biol 28:529–538CrossRefGoogle Scholar
  254. Tewari RK, Kumar P, Sharma PN (2009) Oxidative stress and antioxidant responses in young leaves of mulberry plants grown under nitrogen, phosphorus or potassium deficiency. J Integr Plant Biol 49:313–322CrossRefGoogle Scholar
  255. Tuteja N (2007) Mechanisms of high salinity tolerance in plants. Methods Enzymol 428:419–438CrossRefGoogle Scholar
  256. Vansuyt G, Lopez F, Inzé D, Briat JF, Fourcroy P (1997) Iron triggers a rapid induction of ascorbate peroxidase gene expression in Brassica napus. FEBS Lett 410:195–200CrossRefGoogle Scholar
  257. Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655CrossRefGoogle Scholar
  258. Wang J, Zhang H, Allen RD (1999) Overexpression of an Arabidopsis peroxisomalascorbate peroxidase gene in tobacco increases protection against oxidative stress. Plant Cell Physiol 40:725–732CrossRefGoogle Scholar
  259. Wang WB, Kim YH, Lee HS, Deng XP, Kwak SS (2009) Differential antioxidation activities in two alfalfa cultivars under chilling stress. Plant Biotechnol Rep 3:301–307CrossRefGoogle Scholar
  260. Warburg O (1923) Ueber die antikatalytische Wirkung der Blaus ure. Biochem Z 136:266–272Google Scholar
  261. Wu T, Hsu Y, Lee T (2009) Effects of cadmium on the regulation of antioxidant enzyme activity, gene expression, and antioxidant defenses in the marine macroalga Ulva fasciata. Bot Stud 50:25–34Google Scholar
  262. Wu H, Liu X, Zhao J, Yu J (2012) Toxicological responses in halophyte Suaeda salsa to mercury under environmentally relevant salinity. Ecotoxicol Environ Saf 85:64–71CrossRefGoogle Scholar
  263. Xing Y, Jia W, Zhang J (2007) AtMEK1 mediates stress-induced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis. J Exp Bot 58:2969–2981CrossRefGoogle Scholar
  264. Xu W, Shi W, Liu F, Ueda A, Takabe T (2008) Enhanced zinc and cadmium tolerance and accumulation in transgenic Arabidopsis plants constitutively overexpressing a barley gene (HvAPX1) that encodes a peroxisomal ascorbate peroxidase. Botany 86:567–575CrossRefGoogle Scholar
  265. Xu SC, Li YP, Hu J, Guan YJ, Ma WG, et al. (2010) Responses of antioxidant enzymes to chilling stress in tobacco seedlings. Agric Sci China 9:594–1601Google Scholar
  266. Yadav P, Yadav T, Kumar S, Rani B, Kumar S, Jain V, Malhotra SP (2014) Partial purification and characterization of ascorbate peroxidase from ripening ber (Ziziphus mauritiana L.) fruits. Afr J Biotechnol 13:3323–3331CrossRefGoogle Scholar
  267. Yamaguchi K, Mori H, Nishimura M (1995a) A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal leaf peroxisomal membranes in pumpkin. Plant Cell Physiol 36:1157–1162Google Scholar
  268. Yamaguchi K, Takeuchi Y, Mori H, Nishimura M (1995b) Development of microbody membrane proteins during the transformation of glyoxysomes to leaf peroxisomes in pumpkin cotyledons. Plant Cell Physiol 36:455–464Google Scholar
  269. Yang T, Poovaiah BW (2002) Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proc Natl Acad Sci 99(6):4097–4102CrossRefGoogle Scholar
  270. Yang F, Xu X, Xiao X, Li C (2009) Responses to drought stress in two poplar species originating from different altitudes. Biol Plant 53:511–516CrossRefGoogle Scholar
  271. Yin L, Wang S, Eltayeb AE, Uddin Md I, Yamamoto Y, et al. (2010) Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231:609–621CrossRefGoogle Scholar
  272. Yoruk IH, Demir H, Ekici K, Sarvan A (2005) Purification and properties of catalase from van apple golden delicious. Pak J Nutr 4:8–10CrossRefGoogle Scholar
  273. Yoshimura K, Ishikawa T, Nakamura Y, Tamoi M, Takeda T, et al. (1998) Comparative study on recombinant chloroplastic and cytosolic ascorbate peroxidase isozymes of spinach. Arch Biochem Biophys 353:55–63CrossRefGoogle Scholar
  274. Yoshimura K, Ishikawa T, Tamoi M, Shigeoka S (1999) Alternatively spliced mRNA variants of chloroplast ascorbate peroxidase isoenzymes in spinach leaves. Biochem J 338:41–48CrossRefGoogle Scholar
  275. Yoshimura K, Yabuta Y, Ishikawa T, Shigeoka S (2002) Identification of a cis element for tissue-specific alternative splicing of chloroplast ascorbate peroxidase pre-mRNA in higher plants. J Biol Chem 277:40623–40632CrossRefGoogle Scholar
  276. Zaharieva T, Abadía J (2003) Iron deficiency enhances the levels of ascorbate, glutathione related enzymes in sugar beet roots. Protoplasma 221:269–275Google Scholar
  277. Zamocky M, Furtmüller PG, Bellei M, Battistuzzi G, Stadlmann J, Vlasits J, Obinger C (2009) Intracellular catalase/peroxidase from the phytopathogenic rice blast fungus Magnaporthe grisea: expression analysis and biochemical characterization of the recombinant protein. Biochem J 418(2):443–451CrossRefGoogle Scholar
  278. Zhang H, Wang J, Nickel U, Allen RD, Goodman HM (1997) Cloning and expression of an Arabidopsis gene encoding a putative peroxisomal ascorbate peroxidase. Plant Mol Biol 34:967–971CrossRefGoogle Scholar
  279. Zhang Z, Zhang Q, Wu J, Zheng X, Zheng S, et al. (2013) Gene knockout study reveals that cytosolic ascorbate peroxidase 2(OsAPX2) plays a critical role in growth and reproduction in rice under drought, salt and cold stresses. PLoS One 8:e57472. doi: 10.1371/journal.pone.0057472 CrossRefGoogle Scholar
  280. Zhang F, Wan X, Zheng Y, Sun L, Chen Q, Zhu X, Guo YL, Liu M (2014) Effects of nitrogen on the activity of antioxidant enzymes and gene expression in leaves of Populus plants subjected to cadmium stress. J Plant Interact 9:599–609CrossRefGoogle Scholar
  281. Zhou CP, Qi YP, You X, Yang LT, Guo P, Ye X, Zhou XX, Ke FJ, Chen LS (2013) Leaf cDNA-AFLP analysis of two citrus species differing in manganese tolerance in response to long-term manganese-toxicity. BMC Genomicc 14(1):1Google Scholar
  282. Zhu Z, Wei G, Li J, Qian Q, Yu J (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167:527–533CrossRefGoogle Scholar
  283. Zimmermann P, Heinlein C, Orendi G, Zentgraf U (2006) Senescence-specific regulation of catalase in Arabidopsis thaliana L. Heynh. Plant Cell Environ 29:1049–1056CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Naser A. Anjum
    • 1
    Email author
  • Pallavi Sharma
    • 2
    Email author
  • Sarvajeet S. Gill
    • 3
  • Mirza Hasanuzzaman
    • 4
  • Ekhlaque A. Khan
    • 2
  • Kiran Kachhap
    • 2
  • Amal A. Mohamed
    • 5
  • Palaniswamy Thangavel
    • 6
  • Gurumayum Devmanjuri Devi
    • 6
  • Palanisamy Vasudhevan
    • 6
  • Adriano Sofo
    • 7
  • Nafees A. Khan
    • 8
  • Amarendra Narayan Misra
    • 2
    Email author
  • Alexander S. Lukatkin
    • 9
  • Harminder Pal Singh
    • 10
  • Eduarda Pereira
    • 1
  • Narendra Tuteja
    • 11
    Email author
  1. 1.CESAM-Centre for Environmental and Marine Studies and Department of ChemistryUniversity of AveiroAveiroPortugal
  2. 2.Centre for Life Sciences, School of Natural SciencesCentral University of JharkhandRanchiIndia
  3. 3.Stress Physiology and Molecular Biology Laboratory, Centre for BiotechnologyMD UniversityRohtakIndia
  4. 4.Department of Agronomy, Faculty of AgricultureSher-e-Bangla Agricultural UniversityDhakaBangladesh
  5. 5.Plant Biochemistry DepartmentNational Research Centre (NRC)DokkiEgypt
  6. 6.Department of Environmental Science, School of Life SciencesPeriyar UniversitySalemIndia
  7. 7.School of Agricultural, Forestry, Food and Environmental SciencesUniversity of BasilicataPotenzaItaly
  8. 8.Department of BotanyAligarh Muslim UniversityAligarhIndia
  9. 9.Department of Botany, Physiology and Ecology of PlantsN.P. Ogarev Mordovia State UniversitySaranskRussia
  10. 10.Department of Environment StudiesPanjab UniversityChandigarhIndia
  11. 11.Amity Institute of Microbial Technology (AIMT)Amity University Uttar PradeshNoidaIndia

Personalised recommendations