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ROS and Oxidative Stress: Origin and Implication

  • Soumen Bhattacharjee
Chapter

Abstract

Molecular oxygen (O2) is the primary cellular electron acceptor in aerobic respiration that serves fundamental roles in membrane-linked ATP formation and other fundamental cellular and metabolic functions. But, as an untoward but inescapable consequence of different metabolic events in oxygen-saturated cellular environment, reactive oxygen species (ROS) are incessantly generated by partial or incomplete reduction of molecular oxygen. In plants, ROS are continuously generated as oxidation – reduction cascades of different metabolism located in different cellular compartments and as by-product of various metabolic events. The most important ROS include superoxide (O2.−), perhydroxy radical (HO2.), hydrogen peroxide (H2O2), hydroxy radical (OH.), and singlet oxygen (O2). The other secondary oxidative products like alkoxy radical (RO.), peroxy radical (ROO.), organic hydroperoxide (ROOH), excited carbonyl (RO.), etc. are also produced in plant cells. Though ROS is generated under natural conditions, their productions are augmented under the exposure of unfavorable environmental cues and natural course of senescence. Major sources of ROS in plant cell encompass spilling of electrons during photosynthetic and respiratory electron transport, decompartmentalization of transition metal ions, and also various biological redox reactions. In fact, the redox cascades of chloroplast, peroxisome, and mitochondria of green cells not only determine the driving forces for metabolism but also recognized as the prime source of ROS. Lipid peroxidation, which is known to produce ROS like alkoxy, peroxy radicals as well as singlet oxygen, is also considered as bona fide source of ROS in plant cells. In plants, apoplastic enzyme respiratory burst oxidase homologs (RBOHs) or NADPH oxidases play a major role in originating ROS wave through the other network of ROS production as well. The ROS wave, which is a consequence of perception of unfavorable environmental cues should be integrated with additional metabolic/signaling pathways to enable rapid systemic acclimation of plants. However, an elaborate and efficient antioxidative defense system, comprising a variety of antioxidant molecules, quenchers, and enzymes, determines the ROS turnover and hence the steady-state level of ROS and the redox status of the cell. Plants are equipped with those defense systems not only to combat enhanced level of ROS but also to tightly regulate the endogenous concentration necessary for controlling various events of Plant Biology. However, the decontrolled level of ROS generation, if remaining unabated may cause a solemn threat to or cause oxidative deterioration and in extreme cases the death of plant cells. The present chapter describes the physicochemical basis of the production of ROS, under normal and unfavorable environmental conditions, and senescence, with an added effort to understand their implication associated with those situations.

Keywords

Oxyfree radicals Oxidative stress Antioxidative defense Environmental stress ROS wave Environmental stress 

References

  1. Allen DJ, McKee IF, Farage PK, Baker NR (1997) Analysis of the limitation to CO2 assimilation on exposure of leaves of two Brassica napus cultivars to UV-B. Plant Cell Environ 20:633–640CrossRefGoogle Scholar
  2. Alscher RG, Hess JL (1993) Antioxidant in higher plants. CRC Press, Boca Raton. ISBN O-8493-6328-4Google Scholar
  3. Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationship in green cells. Physiol Plant 100:224–233CrossRefGoogle Scholar
  4. Andreyev AY, Kushnareva YE, Starkov AA (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry 70:200–214PubMedGoogle Scholar
  5. Apel K, Hirt H (2004) Reactive oxygen species; metabolism, oxidative stress and signal transduction. Ann Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  6. Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Curr Sci 82(10):1227–1273Google Scholar
  7. Asada K (1999) The water-water cycle in chloroplast:scavenging oxygens and dissipation of excess protons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639CrossRefPubMedPubMedCentralGoogle Scholar
  8. Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmund CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 227–287Google Scholar
  9. Aust SD, Moorehouse CE, Thomas CE (1985) Role of metals in oxygen radical reactions. J Free Radic Biol Med 01:03–25CrossRefGoogle Scholar
  10. Bartoli CG, Simontacchi M, Eduardo T, Beltrano J, Montaldi E, Puntarulo S (1999) Drought and watering-dependent oxidative stress: effect on antioxidant content in Triticum aestivum L. leaves. J Exp Bot 50(332):375–383CrossRefGoogle Scholar
  11. Bhattacharjee S (1998) Membrane lipid peroxidation, free radical scavengers and ethylene evolution in Amaranthus as affected by lead and cadmium. Biol Plant 40(1):131–135CrossRefGoogle Scholar
  12. Bhattacharjee S (2005) Reactive oxygen species and oxidative burst: role in stress, senescence and signal transduction in plants. Curr Sci 89(05):1115–1121Google Scholar
  13. Bhattacharjee S (2008) Calcium –dependent signaling pathway in the heat induced oxidative injury in Amaranthus lividus L. Biol Plant 52(01):137–140CrossRefGoogle Scholar
  14. Bhattacharjee S (2012) An inductive pulse of hydrogen peroxide pretreatment restores redox- homeostasis and mitigates oxidative membrane damage under extremes of temperature in two rice cultivars (Oryza sativa L., cultivars Ratna and SR 26B). Plant Growth Regul 68:395–410CrossRefGoogle Scholar
  15. Bhattacharjee S (2014) Membrane lipid peroxidation and its conflict of interest: the two faces of oxidative stress. Curr Sci 107:1811–1823Google Scholar
  16. Bhattacharjee S, Mukherjee AK (1996) Lead and cadmium mediated membrane damage in Rice. II. Hydrogen peroxide level, superoxide-dismutase, catalase and peroxidase activities. J Ecotoxicol Environ Monit 06(01):035–039Google Scholar
  17. Bhattacharjee S, Mukherjee AK (2001) Abiotic stress induced membrane damage in plants: a free radical phenomenon. In: Pandey SK (ed) Advances of stress physiology of plants. Scientific Publishers of India, Jhodpur, pp 16–36Google Scholar
  18. Bhattacharjee S, Mukherjee AK (2002) Salt stress induced cytosolute accumulation, antioxidant response and membrane deterioration in three rice cultivars during germination. Seed Sci Technol 30:279–287Google Scholar
  19. Bhattacharjee S, Mukherjee AK (2003) Implication of reactive oxygen species in heat shock induced germination and early growth impairment in Amaranthus lividus L. Biol Plant 47(04):517–522CrossRefGoogle Scholar
  20. Bhattacharjee S, Mukherjee AK (2004) Heavy metal induced germination and early growth impairment in Amaranthus lividus L.: implications of oxidative membrane damage. J Plant Biol 31(1):01–11Google Scholar
  21. Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory: primary compounds secondary metabolites and ROS as components of induced resistance. J Chem Ecol 21:1511–1530CrossRefGoogle Scholar
  22. Biehler K, Fock H (1996) Evidence for the contribution of the Mehler-peroxidase reaction in dissipating excess electrons in drought-stressed wheat. Plant Physiol 112:265–272CrossRefPubMedPubMedCentralGoogle Scholar
  23. Bolwell GP, Bnti VS, Davis DR, Zinmorlin A (1995) The origin of oxidative burst in plants. Free Radic Res 23:517–532CrossRefGoogle Scholar
  24. Borchman D, Sinha S (2002) Determination of products of lipid oxidation by infrared spectroscopy. In: Armstrong D (ed) Oxidative stress biomarkers and antioxidant protocols. Humana Press Inc, Totowa, pp 21–28CrossRefGoogle Scholar
  25. Boveris A, Cadenas E (1975) Mitochondrial production of superoxide anions and its relationship to the antimycin insensitive respiration. FEBS Lett 54(3):311–314CrossRefGoogle Scholar
  26. Bowler C, Van Camp W, Van Montagu M, Inzé D (1994) Superoxide dismutases in plants. Crit Rev Plant Sci 13:199–218CrossRefGoogle Scholar
  27. Brady JD, Fry SC (1997) Formation of di–isodityrosine and loss of isodityrosine in cell walls of tomato of cell suspension cultures treated with fungal elicitors or hydrogen peroxide. Plant Physiol 115:87–92CrossRefPubMedPubMedCentralGoogle Scholar
  28. Bruke JJ, Gamble PE, Hatfield JL, Quinsberry JE (1985) Morphological and biochemical responses to field water deficit. I. Responses to glutathione reductase activity and paraquat sensitivity. Plant Physiol 79:415–419CrossRefGoogle Scholar
  29. Buchanon BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220CrossRefGoogle Scholar
  30. Chen SX, Schopfer P (1999) Hydroxyl radical production in physiological reactions: a novel function of peroxidase. Eur J Biochem 260:726–735CrossRefPubMedPubMedCentralGoogle Scholar
  31. Chowdhury FK, Rivero FM, Blumwald E, Mittler R (2016) Reactive oxygen species, abiotic stress and stress combination. Plant J.  https://doi.org/10.1111/tpj.13299
  32. Cressien G, Firmin J, Fryer M, Kular B, Leyland N (1999) Elevated glutathione biosynthesis capacity in the chloroplast of transgenic tobacco plants paradoxically causes increased oxidative stress. Plant Cell 11:1277–1292CrossRefGoogle Scholar
  33. Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53CrossRefGoogle Scholar
  34. Dat J, Van Breusegerm F, Vandenabeele S, Vranova E, Van Montagu M, Inze D (2000) Active oxygen species and catalase during plant stress response. Cell Mol Life Sci 57:779–786CrossRefPubMedPubMedCentralGoogle Scholar
  35. Davison PA, Hunter CN, Horton P (2002) Overexpression of β-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418:203–206CrossRefPubMedPubMedCentralGoogle Scholar
  36. De Groot JJMC, Veldink GA, Vliegenthart JFG, Bpldingh J, Wever R, Vangelder BF (1975) Demonstration by EPR spectroscopy of functional role of iron in soybean lipoxygenase 1. Biochem Biophys Acta 377:71–79PubMedPubMedCentralGoogle Scholar
  37. Del Rio LA, Sandalio LM, Palma JM, Bueno P, Cospus FJ (1992) Metabolism of oxygen radicals in peroxisomes and cellular implications. Free Radic Biol Med 13:557–580CrossRefPubMedPubMedCentralGoogle Scholar
  38. Devlin WS, Gustine DL (1992) Involvement of oxidative burst in phytoallexin accumulation and hypersensitive reaction. Plant Physiol 100:1189–1195CrossRefPubMedPubMedCentralGoogle Scholar
  39. Dhindsa RJ, Dhindsa PP, Thorpe TA (1982) Leaf senescence and lipid peroxidation: effect of some phytohormones and scavengers of free radicals and singlet oxygen. Physiol Plant 56:543–557CrossRefGoogle Scholar
  40. Doke N, Miura Y, Leandro MS, Kawakitn K (1994) Involvement of superoxide in signal transduction: responses to attack pathogens, physical and chemical shocks and UV irradiation. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defense systems in plants. CRC Press, Boca Raton, pp 177–197Google Scholar
  41. Drerup MM, Schlücking K, Hashimoto K, Manishankar P, Steinhorst L, Kuchitsu K (2013) The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant 6:559–569CrossRefPubMedPubMedCentralGoogle Scholar
  42. Dutilleul C, Garmier M, Noctor G, Mathieu CD, Chetrit P, Foyer CH, De paepe R (2003) Leaf mitochondria modulate whole cell redox homoeostasis, set antioxidant capacity and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15:1212–1226CrossRefPubMedPubMedCentralGoogle Scholar
  43. Eltsner EF (1982) Oxygen activation and oxygen toxicity. Annu Rev Plant Physiol 33:73–96CrossRefGoogle Scholar
  44. Eltsner EF (1987) Metabolism of activated oxygen species. In: Davis D (ed) The biochemistry of plants San Diego. Academic Press, pp 253–315Google Scholar
  45. Evans NH, McAinsh MR, Hetherington AM, Knight MR (2005) ROS perception in Arabidopsis thaliana: the ozone-induced calcium response. Plant J 41:615–626.  https://doi.org/10.1111/j.1365-313X.2004.02325.xCrossRefPubMedPubMedCentralGoogle Scholar
  46. Fadzillah NM, Gill V, Flinch RP, Burdon RH (1996) Chilling, oxidative stress and antioxidative response in shoot cultivars of rice. Planta 199:552–556CrossRefGoogle Scholar
  47. Forman HJ, Boveris A (1982) Free radicals in biology and medicine, vol 5. Academic Press, New York, pp 65–90CrossRefGoogle Scholar
  48. Foyer CH (1997) Oxygen metabolism and electron transport in in photosynthesis. In: Scandalios J (ed) Molcular biology of free radical scavenging enzymes. Cold Spring Harbor Laboratory, New YorkGoogle Scholar
  49. Foyer CH, Harbinson J (1994) Oxygen metabolism and regulation of photoelectron transport. In: Foyer CH, Mullineauex PM (eds) Causes of photooxidative stress and amelioration of defense systems in plants. CRC Press, Boca Raton, pp 01–13Google Scholar
  50. Foyer CH, Noctor G (2003) Redox sensing and signaling associated with reactive oxygen in chloroplast, peroxysome and mitochondria. Physiol Plant 119:355–364CrossRefGoogle Scholar
  51. Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100CrossRefPubMedPubMedCentralGoogle Scholar
  52. Fridovich I (1986) Superoxide dismutases. Adv Enzymol Relat Areas Mol Biol 58:61–97PubMedPubMedCentralGoogle Scholar
  53. Fridovich I (1995) Superoxide and superoxide dismutase. Ann Rev Biochem 64:97–112CrossRefPubMedPubMedCentralGoogle Scholar
  54. Gabig TG (1983) NADPH-dependent superoxide generating oxidase from human nutrophils. J Biol Chem 258:6352–6356PubMedPubMedCentralGoogle Scholar
  55. Gill SS, Khan NA, Anjum NA, Tuteja N (2011) Amelioration of cadmium stress in crop plants by nutrients management: morphological, physiological and biochemical aspects. In: Anjum NA, Lopez-Lauri F (eds) Plant nutrition and abiotic stress tolerance III, plant stress 5 (Special Issue 1). Global Science Books Ltd.), Ikenobe, pp 1–23Google Scholar
  56. Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19:623–630CrossRefPubMedPubMedCentralGoogle Scholar
  57. Grossman S, Leshem YY (1978) Lowering endogenous LOX activities in Pisum sativum by cytokinin as related to senescence. Physiol Plant 43:359–362CrossRefGoogle Scholar
  58. Halliwell B (2006) Reactive species and antioxidants: Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322CrossRefPubMedPubMedCentralGoogle Scholar
  59. Halliwell B, Gutteridge JMC (1984) Oxygen toxicity and oxyradicals, transition metals and disease. Biochem J 219:01–19CrossRefGoogle Scholar
  60. Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine, 3rd edn. Oxford University Press, New YorkGoogle Scholar
  61. Hameed A, Goher M, Iqbal N (2013) Drought induced programmed cell death and associated changes in antioxidants, proteases, and lipid peroxidation in wheat leaves. Biol Plant 57:370–374CrossRefGoogle Scholar
  62. Hammond-Kosack KE, Jones JDC (2000) Responses to plant pathogen. In: Buchanon BB, Grussem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiology, Rockville, pp 102–106Google Scholar
  63. Han D, Ybanez MD, Ahmadi S, Yeh K, Kaplowitz N (2009) Redox regulation of tumor necrosis factor signaling. Antioxid Redox Signal 11:2245–2263CrossRefPubMedPubMedCentralGoogle Scholar
  64. Hendry GAF, Baker AJM, Ewart CF (1992) Cadmium tolerance and toxicity, oxygen radical processes and molecular damages in cadmium tolerant and sensitive clones of Holcuslanatus. Acta Bot Mecrl 41:271–281CrossRefGoogle Scholar
  65. Hernández JA, Jiménez A, Mullineaux P, Sevilla F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defenses. Plant Cell Environ 23:853–862doi.  https://doi.org/10.1046/j.1365-3040.2000.00602.xCrossRefGoogle Scholar
  66. Hideg E, Kalai T, Hideg K, Vass L (1998) Photoinhibition of photosynthesis in vivo results in singlet oxygen production. Detection via nitroxide induced fluorescence quenching in broad bean leaves. Biochemistry 37:11405–11411CrossRefPubMedPubMedCentralGoogle Scholar
  67. Hideg E, Barta C, Kalai T, Hideg K, Vass L, Asada K (2002) Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol 11:54–64Google Scholar
  68. Higuchi T (2006) Look back over the studies of lignin biochemistry. J Wood Sci 52:2.  https://doi.org/10.1007/s10086-005-0790-zCrossRefGoogle Scholar
  69. Imlay JA (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77:755–776CrossRefPubMedPubMedCentralGoogle Scholar
  70. Jabs T (1999) Reactive oxygen species intermediates as mediators of programmed cell eath in plants and animals. Biochem Pharmacol 57:231–245CrossRefGoogle Scholar
  71. Jiang M, Zhang J (2001) Effect of ABA on active oxygen species, antioxidative defense system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42(11):1265–1273CrossRefGoogle Scholar
  72. Kimura S, Kaya H, Kawarazaki T, Hiraoka G, Senzaki E, Michikawa M (2012) Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochim Biophys Acta 1823:398–405.  https://doi.org/10.1016/j.bbamcr.2011.09.011CrossRefPubMedGoogle Scholar
  73. Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346.  https://doi.org/10.1093/jxb/erh237CrossRefPubMedGoogle Scholar
  74. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL (2003) NADPH oxidase Atrboh D and Atrboh F genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633.  https://doi.org/10.1093/emboj/cdg277CrossRefPubMedPubMedCentralGoogle Scholar
  75. Laloi C, Apel K, Danon A (2004) Reactive oxygen signaling: the latest news. Curr Opin Plant Biol 7:323–328CrossRefGoogle Scholar
  76. Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275CrossRefPubMedPubMedCentralGoogle Scholar
  77. Legendre L, Rueter S, Heinstei PF, Low PS (1993) Characterization of the oligogacturroxide-induced oxidative burst in cultured soybean cells. Plant Physiol 102:233–240CrossRefPubMedPubMedCentralGoogle Scholar
  78. Levine A (1999) Oxidative stress as regulator environmental responses in plants. In: Ferver HR (ed) Plant responses to environmental stress. Mervel Decker Inc, Switzerland, pp 146–163Google Scholar
  79. Levine A, Tenhaken R, Dixon R, Lamb CJ (1994) Hydrogen peroxide from oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593CrossRefGoogle Scholar
  80. Levine A, Pennell RI, Alvarez MF, Palmer R, Lamb C (1996) Calcium mediated apoptosis in a plant hypersensitive disease response. Curr Biol 04:427–437CrossRefGoogle Scholar
  81. Lin F, Ding H, Wang J, Zhang H, Zhang A, Zhang Y (2009) Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J Exp Bot 60:3221–3238.  https://doi.org/10.1093/jxb/erp157CrossRefPubMedPubMedCentralGoogle Scholar
  82. Mahalingam R, Fredroff N (2003) Stress response, cell death and signaling: the many faces of ROS. Physiol Plant 119:56–68CrossRefGoogle Scholar
  83. Maxwell DP, Wang Y, McIntosh L (1999) Alternative oxidase lowers mitochondrial ROS production in plant cells. Proc Natl Acad Sci 96:8271–8276CrossRefGoogle Scholar
  84. Maxwell DP, Nickels R, McIntosch L (2002) Evidence of mitochondrial involvement in transduction of signals required for induction of genes associated with pathogen attack and senescence. Plant J 29:269–279CrossRefGoogle Scholar
  85. Mehlar AH (1951) Studies on reactions of Illuminated chloroplasts. II Stimulation and inhibition of reaction b with oxygen. Arch Biochem Biophys 33:65–77CrossRefGoogle Scholar
  86. Millar AH, Leaver CJ (2000) The cytotoxic lipid peroxidation product, 4-hydroxyl-2-nonenal specifically inhibits dehydrogenase in matrix of plant mitochondria. FEBS Lett 481:117–121CrossRefGoogle Scholar
  87. Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133(3):481–489CrossRefGoogle Scholar
  88. Miller G, Schlauch K, Tam R, Cortes D, Torres MA (2009) The plant NADPH oxidase RbohD mediates rapid, systemic signaling in response to diverse stimuli. Sci Signal 2(84):45–49CrossRefGoogle Scholar
  89. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:453–467CrossRefPubMedPubMedCentralGoogle Scholar
  90. Mittler R (2017) ROS are good. Trends Plant Sci 22(1):11–19Google Scholar
  91. Mittler R, Blumwald E (2015) The roles of ROS and ABA in systemic acquired acclimation. Plant Cell 27:64–70.  https://doi.org/10.1105/tpc.114.133090CrossRefPubMedPubMedCentralGoogle Scholar
  92. Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications of cellular proteins. Annu Rev Plant Biol 58:459–481CrossRefGoogle Scholar
  93. Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417(1):1–13.  https://doi.org/10.1042/BJ20081386CrossRefPubMedGoogle Scholar
  94. Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol:5388–5395.  https://doi.org/10.1016/S1369-5266(02)00282-0
  95. Nixon PJ (2000) Chlororespiration. Philos Trans R Soc London 355:1541–1547CrossRefGoogle Scholar
  96. Noctor G, Veljovic-Jovanovic SD, Driscoll S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in wheat leaves. A predominant role for photorespiration? Ann Bot 89:841–850CrossRefPubMedPubMedCentralGoogle Scholar
  97. Ogawa K, Kanematsu S, Asada K (1997) Generation of superoxide anion and location of Cu-Zn SOD in the vascular tissues of spinach hypodermis and their association with lignification. Plant Cell Physiol 38:1118–1123CrossRefGoogle Scholar
  98. Overmyer K, Brosché M, Kangaskärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342.  https://doi.org/10.1016/S1360-1385(03)00135-3CrossRefPubMedGoogle Scholar
  99. Pei ZM, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734CrossRefGoogle Scholar
  100. Pinto E, Sigaud-kutner T, Leitao MA, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal-induced oxidative stress in algae. J Phycol 39:1008–1018.  https://doi.org/10.1111/j.0022-3646.2003.02-193.xCrossRefGoogle Scholar
  101. Porter NA, Caldwell SE, Mills KA (1995) Mechanisms of free radical oxidation of unsaturated lipids. Lipids 30:277–290.  https://doi.org/10.1007/BF02536034CrossRefPubMedGoogle Scholar
  102. Prasad TK, Anderson MD, Martin B, Stewart CR (1994) Evidence of chilling induced oxidative stress and a regulatory role of hydrogen peroxide. Plant Cell 06:65–74CrossRefGoogle Scholar
  103. Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110:125–136CrossRefPubMedPubMedCentralGoogle Scholar
  104. Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species – contribution to oxidative stress and interorganellar signaling. Plant Physiol 141:357–366CrossRefPubMedPubMedCentralGoogle Scholar
  105. Robson CA, Vanlerberghe GC (2002) Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria –dependent and independent pathways of cell death. Plant Physiol 129:1908–1920CrossRefPubMedPubMedCentralGoogle Scholar
  106. Rouhier N, Stephane D, Lenaire JPJ (2008) The role of glutathione in photosynthetic organism: emerging function of glutaredoxin and glutathionylation. Annu Rev Plant Biol 59:143–166CrossRefGoogle Scholar
  107. Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91(phox) NADPH oxidase: modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290CrossRefPubMedPubMedCentralGoogle Scholar
  108. Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014CrossRefGoogle Scholar
  109. Segal AW, Abo A (1993) The biochemical basis of NADPH oxidase of phagocytes. Trends Biochem Sci 18:43–47CrossRefGoogle Scholar
  110. 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:1–26.  https://doi.org/10.1155/2012/217037
  111. Sharma R, Priya P, Jain M (2013) Modified expression of an auxin-responsive rice CC-type glutaredoxin gene affects multiple abiotic stress responses. Planta 238:871–884CrossRefGoogle Scholar
  112. Sochor J, Babula P, Adam V, Krska B, Kizek R (2012) Sharka: the past, the present and the future. Viruses 4:2853–2901CrossRefPubMedPubMedCentralGoogle Scholar
  113. Somashekaraiah BV, Padmaja K, Prasad ARK (1992) Phytotoxicity of cadmium ions on germinating seedlings of mungbean (Phaseolus vulgaris): involvement of lipid peroxides in chlorophyll degradation. Physiol Plant 85:85–89CrossRefGoogle Scholar
  114. Spiteller G (2003) The relationship between cell wall, lipid peroxidation, proliferation, senescence and cell death. Physiol Plant 119:05–18CrossRefGoogle Scholar
  115. Spreitzer H, Schmidt J, Spiteller G (1989) Comparative analyses of the fatty acid fraction of vegetables in dependence on preliminary treatment. Fett Wiss Technol 91:108–113Google Scholar
  116. Strid A, Chow WS, Anderson JM (1994) UV-B damage and protection at the molecular level in plants. Photosynth Res 39:475–489CrossRefGoogle Scholar
  117. Suzuki N, Koussevitzky S, Mittler R, Miller G (2011) ROS and redox signaling in response to abiotic stress. Plant Cell Environ.  https://doi.org/10.1111/j.1365-3040.2011.02336.x
  118. Suzuki N, Miller G, Salazar C, Mondal HA, Shulaev E, Cortes DF (2013) Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 25:3553–3569.  https://doi.org/10.1105/tpc.113.114595CrossRefPubMedPubMedCentralGoogle Scholar
  119. Thompson JE, Legge RE, Barber RF (1987) Role of free radicals in senescence and wounding. New Phytol 105:313–344CrossRefGoogle Scholar
  120. Torres MA, Dangl JL, Jones JDG (2002) Arabidopsis gp91 phox homologues atrboh D atrboh F are required for acclimation reactive oxygen intermediates in plant dependent response. Proc Natl Acad Sci U S A 99:517–522CrossRefGoogle Scholar
  121. Van Assche F, Clijsters H (1990) Effect of metals on enzymic activity in plants. Plant Cell Environ 13:195–206CrossRefGoogle Scholar
  122. Vanova E, VanBreusegerm F, Dat J, Belles-Bolx E, Inze D (2002) Role of reactive oxygen species in signal transduction. In: Scheel D, Wasternack C (eds) Plant signal transduction. Oxford University Press, Oxford, pp 41–73Google Scholar
  123. Winston GW (1990) Physicochemical basis of free radical formation in cells: production and defenses. In: Smallwood W (ed) Stress responses in plants: adaptation and acclimation mechanisms. Willy-Liss Inc, New York, pp 57–86Google Scholar
  124. Wiseman H, Halliwell B (1996) Damage to DNA by reactive oxygen species and nitrogen species. Cancer Biochem J 387:856–870Google Scholar
  125. Zhou YH, Yu JQ, Mao WH, Huang LF, Song XS, Nogués S (2006) Genotypic variation on Rubisco expression, photosynthetic electron flow and antioxidant metabolism in the chloroplasts of chill-exposed cucumber plants. Plant Cell Physiol 47:192–199CrossRefGoogle Scholar

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© Springer Nature India Private Limited 2019

Authors and Affiliations

  • Soumen Bhattacharjee
    • 1
  1. 1.Department of BotanyUGC Centre for Advanced Study, The University of BurdwanBurdwanIndia

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