Reactive oxygen species (ROS) are produced as a normal product of plant cellular metabolism. Various environmental stresses lead to excessive production of ROS causing progressive oxidative damage and ultimately cell death. Despite their destructive activity, they are well-described second messengers in a variety of cellular processes, including conferment of tolerance to various environmental stresses. Whether ROS would serve as signaling molecules or could cause oxidative damage to the tissues depends on the delicate equilibrium between ROS production, and their scavenging. Efficient scavenging of ROS produced during various environmental stresses requires the action of several nonenzymatic as well as enzymatic antioxidants present in the tissues. In this paper, we describe the generation, sites of production and role of ROS as messenger molecules as well as inducers of oxidative damage. Further, the antioxidative defense mechanisms operating in the cells for scavenging of ROS overproduced under various stressful conditions of the environment have been discussed in detail. 1. Introduction An unavoidable consequence of aerobic metabolism is production of reactive oxygen species (ROS). ROS include free radicals such as superoxide anion ( O 2 ？ ？ ), hydroxyl radical (？OH), as well as nonradical molecules like hydrogen peroxide (H2O2), singlet oxygen (1O2), and so forth. Stepwise reduction of molecular oxygen (O2) by high-energy exposure or electron-transfer reactions leads to production of the highly reactive ROS. In plants, ROS are always formed by the inevitable leakage of electrons onto O2 from the electron transport activities of chloroplasts, mitochondria, and plasma membranes or as a byproduct of various metabolic pathways localized in different cellular compartments [1–5]. Environmental stresses such as drought, salinity, chilling, metal toxicity, and UV-B radiation as well as pathogens attack lead to enhanced generation of ROS in plants due to disruption of cellular homeostasis [6–15]. All ROS are extremely harmful to organisms at high concentrations. When the level of ROS exceeds the defense mechanisms, a cell is said to be in a state of “oxidative stress.” The enhanced production of ROS during environmental stresses can pose a threat to cells by causing peroxidation of lipids, oxidation of proteins, damage to nucleic acids, enzyme inhibition, activation of programmed cell death (PCD) pathway and ultimately leading to death of the cells [6–8, 11, 13, 14, 16, 17]. Despite their destructive activity, ROS are well-described second messengers in a
References
[1]
C. H. Foyer and J. Harbinson, “Oxygen metabolism and the regulation of photosynthetic electron transport,” in Causes of Photooxidative Stresses and Amelioration of Defense Systems in Plants, C. H. Foyer and P. Mullineaux, Eds., pp. 1–42, CRC Press, Boca Raton, Fla, USA, 1994.
[2]
C. H. Foyer, “Oxygen metabolism and electron transport in photosynthesis,” in Molecular Biology of Free Radical Scavenging Systems, J. Scandalios, Ed., pp. 587–621, Cold Spring Harbor Laboratory Press, New York, NY, USA, 1997.
[3]
L. A. Del Río, L. M. Sandalio, F. J. Corpas, J. M. Palma, and J. B. Barroso, “Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling,” Plant Physiology, vol. 141, no. 2, pp. 330–335, 2006.
[4]
O. Blokhina and K. V. Fagerstedt, “Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems,” Physiologia Plantarum, vol. 138, no. 4, pp. 447–462, 2010.
[5]
E. Heyno, V. Mary, P. Schopfer, and A. Krieger-Liszkay, “Oxygen activation at the plasma membrane: relation between superoxide and hydroxyl radical production by isolated membranes,” Planta, vol. 234, no. 1, pp. 35–45, 2011.
[6]
K. Shah, R. G. Kumar, S. Verma, and R. S. Dubey, “Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings,” Plant Science, vol. 161, no. 6, pp. 1135–1144, 2001.
[7]
R. Mittler, “Oxidative stress, antioxidants and stress tolerance,” Trends in Plant Science, vol. 7, no. 9, pp. 405–410, 2002.
[8]
P. Sharma and R. S. Dubey, “Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings,” Plant Growth Regulation, vol. 46, no. 3, pp. 209–221, 2005.
[9]
W. H. Hu, X. S. Song, K. Shi, X. J. Xia, Y. H. Zhou, and J. Q. Yu, “Changes in electron transport, superoxide dismutase and ascorbate peroxidase isoenzymes in chloroplasts and mitochondria of cucumber leaves as influenced by chilling,” Photosynthetica, vol. 46, no. 4, pp. 581–588, 2008.
[10]
C. Han, Q. Liu, and Y. Yang, “Short-term effects of experimental warming and enhanced ultraviolet-B radiation on photosynthesis and antioxidant defense of Picea asperata seedlings,” Plant Growth Regulation, vol. 58, no. 2, pp. 153–162, 2009.
[11]
R. Maheshwari and R. S. Dubey, “Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings,” Plant Growth Regulation, vol. 59, no. 1, pp. 37–49, 2009.
[12]
G. Tanou, A. Molassiotis, and G. Diamantidis, “Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity,” Environmental and Experimental Botany, vol. 65, no. 2-3, pp. 270–281, 2009.
[13]
S. Mishra, A. B. Jha, and R. S. Dubey, “Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings,” Protoplasma, vol. 248, no. 3, pp. 565–577, 2011.
[14]
S. Srivastava and R. S. Dubey, “Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings,” Plant Growth Regulation, pp. 1–16, 2011.
[15]
P. Sharma and R. S. Dubey, “Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum,” Plant Cell Reports, vol. 26, no. 11, pp. 2027–2038, 2007.
[16]
S. Verma and R. S. Dubey, “Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants,” Plant Science, vol. 164, no. 4, pp. 645–655, 2003.
[17]
B. Meriga, B. K. Reddy, K. R. Rao, L. A. Reddy, and P. B. K. Kishor, “Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa),” Journal of Plant Physiology, vol. 161, no. 1, pp. 63–68, 2004.
[18]
R. Desikan, S. A.-H.-Mackerness S., J. T. Hancock, and S. J. Neill, “Regulation of the Arabidopsis transcriptome by oxidative stress,” Plant Physiology, vol. 127, no. 1, pp. 159–172, 2001.
[19]
S. Neill, R. Desikan, and J. Hancock, “Hydrogen peroxide signalling,” Current Opinion in Plant Biology, vol. 5, no. 5, pp. 388–395, 2002.
[20]
J. Yan, N. Tsuichihara, T. Etoh, and S. Iwai, “Reactive oxygen species and nitric oxide are involved in ABA inhibition of stomatal opening,” Plant, Cell and Environment, vol. 30, no. 10, pp. 1320–1325, 2007.
[21]
G. Noctor and C. H. Foyer, “Ascorbate and glutathione: keeping active oxygen under control,” Annual Review of Plant Biology, vol. 49, pp. 249–279, 1998.
[22]
M. Zaefyzadeh, R. A. Quliyev, S. M. Babayeva, and M. A. Abbasov, “The effect of the interaction between genotypes and drought stress on the superoxide dismutase and chlorophyll content in durum wheat landraces,” Turkish Journal of Biology, vol. 33, no. 1, pp. 1–7, 2009.
[23]
Q. Chen, M. Zhang, and S. Shen, “Effect of salt on malondialdehyde and antioxidant enzymes in seedling roots of Jerusalem artichoke (Helianthus tuberosus L.),” Acta Physiologiae Plantarum, vol. 33, no. 2, pp. 273–278, 2010.
[24]
R. D. Allen, R. P. Webb, and S. A. Schake, “Use of transgenic plants to study antioxidant defenses,” Free Radical Biology and Medicine, vol. 23, no. 3, pp. 473–479, 1997.
[25]
M. Faize, L. Burgos, L. Faize et al., “Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress,” Journal of Experimental Botany, vol. 62, no. 8, pp. 2599–2613, 2011.
[26]
Y. P. Lee, S. H. Kim, J. W. Bang, H. S. Lee, S. S. Kwak, and S. Y. Kwon, “Enhanced tolerance to oxidative stress in transgenic tobacco plants expressing three antioxidant enzymes in chloroplasts,” Plant Cell Reports, vol. 26, no. 5, pp. 591–598, 2007.
[27]
K. Asada and M. Takahashi, “Production and scavenging of active oxygen in photosynthesis,” in Photoinhibition: Topics of Photosynthesis, D. J. Kyle, C. B. Osmond, and C. J. Arntzen, Eds., pp. 227–287, Elsevier, Amsterdam, The Netherlands, 9th edition, 1987.
[28]
K. Apel and H. Hirt, “Reactive oxygen species: metabolism, oxidative stress, and signal transduction,” Annual Review of Plant Biology, vol. 55, pp. 373–399, 2004.
[29]
A. Krieger-Liszkay, “Singlet oxygen production in photosynthesis,” Journal of Experimental Botany, vol. 56, no. 411, pp. 337–346, 2005.
[30]
S. Hatz, J. D. C. Lambert, and P. R. Ogilby, “Measuring the lifetime of singlet oxygen in a single cell: addressing the issue of cell viability,” Photochemical and Photobiological Sciences, vol. 6, no. 10, pp. 1106–1116, 2007.
[31]
S. Hackbarth, J. Schlothauer, A. Preu？, and B. R？der, “New insights to primary photodynamic effects—singlet oxygen kinetics in living cells,” Journal of Photochemistry and Photobiology B, vol. 98, no. 3, pp. 173–179, 2010.
[32]
D. Wagner, D. Przybyla, R. Op Den Camp et al., “The genetic basis of singlet oxygen-induced stress response of Arabidopsis thaliana,” Science, vol. 306, no. 5699, pp. 1183–1185, 2004.
[33]
H. Kasai, “Analysis of a form of oxidative DNA damage, 8-hydroxy-2'-deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis,” Mutation Research, vol. 387, no. 3, pp. 147–163, 1997.
[34]
A. Krieger-Liszkay, C. Fufezan, and A. Trebst, “Singlet oxygen production in photosystem II and related protection mechanism,” Photosynthesis Research, vol. 98, no. 1-3, pp. 551–564, 2008.
[35]
B. Halliwell and J. M. C. Gutteridge, “Oxygen toxicity, oxygen radicals, transition metals and disease,” Biochemical Journal, vol. 219, no. 1, pp. 1–14, 1984.
[36]
M. Valko, H. Morris, and M. T. D. Cronin, “Metals, toxicity and oxidative stress,” Current Medicinal Chemistry, vol. 12, no. 10, pp. 1161–1208, 2005.
[37]
B. Halliwell, “Generation of hydrogen peroxide, superoxide and hydroxyl radicals during the oxidation of dihydroxyfumaric acid by peroxidase,” Biochemical Journal, vol. 163, no. 3, pp. 441–448, 1977.
[38]
J. A. Imlay, “Pathways of oxidative damage,” Annual Review of Microbiology, vol. 57, pp. 395–418, 2003.
[39]
J. M. McCord, J. D. Crapo, and I. Fridovich, “Superoxide dismutase assay. a review of methodology,” in Superoxide and Superoxide Dismutase, A. M. Michelson, J. M. McCord, and I. Fridovich, Eds., pp. 11–17, Academic press, London, UK, 1977.
[40]
R. Mittler and B. A. Zilinskas, “Purification and characterization of pea cytosolic ascorbate peroxidase,” Plant Physiology, vol. 97, no. 3, pp. 962–968, 1991.
[41]
G. P. Bienert, A. L. B. M？ller, K. A. Kristiansen et al., “Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes,” Journal of Biological Chemistry, vol. 282, no. 2, pp. 1183–1192, 2007.
[42]
M. A. Torres, J. L. Dangl, and J. D. G. Jones, “Arabidopsis gp91phox homologues Atrbohd and Atrbohf are required for accumulation of reactive oxygen intermediates in the plant defense response,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 1, pp. 517–522, 2002.
[43]
B. Halliwell and J. M. C. Gutteridge, Free Radicals in Biology and Medicine, Oxford University Press, Oxford, UK, 2rd edition, 1989.
[44]
W. M. Kaiser, “Reversible inhibition of the calvin cycle and activation of oxidative pentose phosphate cycle in isolated intact chloroplasts by hydrogen peroxide,” Planta, vol. 145, no. 4, pp. 377–382, 1979.
[45]
R. C. Leegood and D. A. Walker, “Regulation of fructose-1,6-bisphosphatase activity in leaves,” Planta, vol. 156, no. 5, pp. 449–456, 1982.
[46]
J. Dat, S. Vandenabeele, E. Vranová, M. Van Montagu, D. Inzé, and F. Van Breusegem, “Dual action of the active oxygen species during plant stress responses,” Cellular and Molecular Life Sciences, vol. 57, no. 5, pp. 779–795, 2000.
[47]
A. Rigo, R. Stevanato, A. Finazzi Agro', and G. Rotilio, “An attempt to evaluate the rate of the Haber Weiss reaction by using radical scavengers,” FEBS Letters, vol. 80, no. 1, pp. 130–132, 1977.
[48]
C. H. Foyer, H. Lopez-Delgado, J. F. Dat, and I. M. Scott, “Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling,” Physiologia Plantarum, vol. 100, no. 2, pp. 241–254, 1997.
[49]
E. Pinto, T. C. S. Sigaud-Kutner, M. A. S. Leit？o, O. K. Okamoto, D. Morse, and P. Colepicolo, “Heavy metal-induced oxidative stress in algae,” Journal of Phycology, vol. 39, no. 6, pp. 1008–1018, 2003.
[50]
H. Ishida, Y. Nishimori, M. Sugisawa, A. Makino, and T. Mae, “The large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase is fragmented into 37-kDa and 16-kDa polypeptides by active oxygen in the lysates of chloroplasts from primary leaves of wheat,” Plant and Cell Physiology, vol. 38, no. 4, pp. 471–479, 1997.
[51]
S. Luo, H. Ishida, A. Makino, and T. Mae, “Fe2+-catalyzed site-specific cleavage of the large subunit of ribulose 1,5-bisphosphate carboxylase close to the active site,” Journal of Biological Chemistry, vol. 277, no. 14, pp. 12382–12387, 2002.
[52]
E. F. Elstner, “Oxygen activation and oxygen toxicity,” Annual Review of Plant Biology, vol. 33, pp. 73–96, 1982.
[53]
E. F. Elstner, “Metabolism of activated oxygen species,” in Biochemistry of Plants, D. D. Davies, Ed., pp. 253–315, Academic Press, London, UK, 1987.
[54]
E. F. Elstner, “Mechanisms of oxygen activation in different compartments of plant cells,” in Active Oxygen/Oxidative Stress and Plant Metabolism, E. J. Pell and K. L. Steffen, Eds., pp. 13–25, American Society of Plant Physiologists, Rockville, Md, USA, 1991.
[55]
R. E. Cleland and S. C. Grace, “Voltammetric detection of superoxide production by photosystem II,” FEBS Letters, vol. 457, no. 3, pp. 348–352, 1999.
[56]
A. Arora, R. K. Sairam, and G. C. Srivastava, “Oxidative stress and antioxidative system in plants,” Current Science, vol. 82, no. 10, pp. 1227–1238, 2002.
[57]
J. F. Turrens, “Mitochondrial formation of reactive oxygen species,” Journal of Physiology, vol. 552, no. 2, pp. 335–344, 2003.
[58]
M. P. Murphy, “How mitochondria produce reactive oxygen species,” Biochemical Journal, vol. 417, no. 1, pp. 1–13, 2009.
[59]
G. Noctor, R. De Paepe, and C. H. Foyer, “Mitochondrial redox biology and homeostasis in plants,” Trends in Plant Science, vol. 12, no. 3, pp. 125–134, 2007.
[60]
A. Y. Andreyev, Y. E. Kushnareva, and A. A. Starkov, “Mitochondrial metabolism of reactive oxygen species,” Biochemistry (Moscow), vol. 70, no. 2, pp. 200–214, 2005.
[61]
A. G. Rasmusson, D. A. Geisler, and I. M. M？ller, “The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria,” Mitochondrion, vol. 8, no. 1, pp. 47–60, 2008.
[62]
A. Baker and A. I. Graham, Plant Peroxisomes: Biochemistry, Cell Biology and Biotechnological Applications, Kluwer Academic Publishers, Dordrecht, The Netherlands, 2002.
[63]
G. Noctor, S. Veljovic-Jovanovic, S. Driscoll, L. Novitskaya, and C. H. Foyer, “Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration?” Annals of Botany, vol. 89, pp. 841–850, 2002.
[64]
E. López-Huertas, F. J. Corpas, L. M. Sandalio, and L. A. Del Río, “Characterization of membrane polypeptides from pea leaf peroxisomes involved in superoxide radical generation,” Biochemical Journal, vol. 337, no. 3, pp. 531–536, 1999.
[65]
J. M. Kwak, I. C. Mori, Z. M. Pei et al., “NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis,” EMBO Journal, vol. 22, no. 11, pp. 2623–2633, 2003.
[66]
G. G. Gross, “Cell wall-bound malate dehydrogenase from horseradish,” Phytochemistry, vol. 16, no. 3, pp. 319–321, 1977.
[67]
C. Martinez, J. L. Montillet, E. Bresson et al., “Apoplastic peroxidase generates superoxide anions in cells of cotton cotyledons undergoing the hypersensitive reaction to Xanthomonas campestris pv. malvacearum 18,” Molecular Plant-Microbe Interactions, vol. 11, no. 11, pp. 1038–1047, 1998.
[68]
M. J. Kim, S. Ciani, and D. P. Schachtman, “A peroxidase contributes to ros production during Arabidopsis root response to potassium deficiency,” Molecular Plant, vol. 3, no. 2, pp. 420–427, 2010.
[69]
P. Wojtaszek, “Oxidative burst: an early plant response to pathogen infection,” Biochemical Journal, vol. 322, no. 3, pp. 681–692, 1997.
[70]
B. G. Lane, “Oxalate, germins, and higher-plant pathogens,” IUBMB Life, vol. 53, no. 2, pp. 67–75, 2002.
[71]
A. Cona, G. Rea, R. Angelini, R. Federico, and P. Tavladoraki, “Functions of amine oxidases in plant development and defence,” Trends in Plant Science, vol. 11, no. 2, pp. 80–88, 2006.
[72]
P. C. Bethke and R. L. Jones, “Cell death of barley aleurone protoplasts is mediated by reactive oxygen species,” Plant Journal, vol. 25, no. 1, pp. 19–29, 2001.
[73]
Jung Hee Joo, Yun Soo Bae, and June Seung Lee, “Role of auxin-induced reactive oxygen species in root gravitropism,” Plant Physiology, vol. 126, no. 3, pp. 1055–1060, 2001.
[74]
G. Miller, V. Shulaev, and R. Mittler, “Reactive oxygen signaling and abiotic stress,” Physiologia Plantarum, vol. 133, no. 3, pp. 481–489, 2008.
[75]
L. Xiong, K. S. Schumaker, and J. K. Zhu, “Cell signaling during cold, drought, and salt stress,” Plant Cell, vol. 14, pp. S165–S183, 2002.
[76]
Y. Cheng and C. Song, “Hydrogen peroxide homeostasis and signaling in plant cells,” Science in China. Series C, Life sciences, vol. 49, no. 1, pp. 1–11, 2006.
[77]
Z. M. Pel, Y. Murata, G. Benning et al., “Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells,” Nature, vol. 406, no. 6797, pp. 731–734, 2000.
[78]
R. Jannat, M. Uraji, M. Morofuji et al., “Roles of intracellular hydrogen peroxide accumulation in abscisic acid signaling in Arabidopsis guard cells,” Journal of Plant Physiology, vol. 168, no. 16, pp. 1919–1926, 2011.
[79]
E. Bahin, C. Bailly, B. Sotta, I. Kranner, F. Corbineau, and J. Leymarie, “Crosstalk between reactive oxygen species and hormonal signalling pathways regulates grain dormancy in barley,” Plant, Cell and Environment, vol. 34, no. 6, pp. 980–993, 2011.
[80]
A. K. Nanda, E. Andrio, D. Marino, N. Pauly, and C. Dunand, “Reactive oxygen species during plant-microorganism early interactions,” Journal of Integrative Plant Biology, vol. 52, no. 2, pp. 195–204, 2010.
[81]
D. F. Klessig, J. Durner, R. Noad et al., “Nitric oxide and salicylic acid signaling in plant defense,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 16, pp. 8849–8855, 2000.
[82]
M. L. Orozco-Cárdenas, J. Narváez-Vásquez, and C. A. Ryan, “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, vol. 13, no. 1, pp. 179–191, 2001.
[83]
L. Denness, J. F. McKenna, C. Segonzac et al., “Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis,” Plant Physiology, vol. 156, no. 3, pp. 1364–1374, 2011.
[84]
T. Yuasa, K. Ichimura, T. Mizoguchi, and K. Shinozaki, “Oxidative stress activates ATMPK6, an Arabidopsis homologue of map kinase,” Plant and Cell Physiology, vol. 42, no. 9, pp. 1012–1016, 2001.
[85]
C. M. Yeh, P. S. Chien, and H. J. Huang, “Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice roots,” Journal of Experimental Botany, vol. 58, no. 3, pp. 659–671, 2007.
[86]
O. Borsani, P. Díaz, M. F. Agius, V. Valpuesta, and J. Monza, “Water stress generates an oxidative stress through the induction of a specific Cu/Zn superoxide dismutase in Lotus corniculatus leaves,” Plant Science, vol. 161, no. 4, pp. 757–763, 2001.
[87]
Z. Zhao, G. Chen, and C. Zhang, “Interaction between reactive oxygen species and nitric oxide in drought-induced abscisic acid synthesis in root tips of wheat seedlings,” Australian Journal of Plant Physiology, vol. 28, no. 10, pp. 1055–1061, 2001.
[88]
N. Smirnoff, “Antioxidant systems and plant response to the environment,” in Environment and Plant Metabolism: Flexibility and Acclimation, N. Smirnoff, Ed., pp. 217–243, Bios Scientific Publishers, Oxford, UK, 1995.
[89]
R. O. Recknagal and E. A. Glende, “Oxygen radicals in biological systems,” in Methods in Enzymology, L. Packer, Ed., vol. 105, pp. 331–337, Academic Press, New York, NY, USA, 1984.
[90]
K. J. A. Davies, “Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems,” IUBMB Life, vol. 50, no. 4-5, pp. 279–289, 2000.
[91]
G. R. Buettner, “The pecking order of free radicals and antioxidants: lipid peroxidation, α-tocopherol, and ascorbate,” Archives of Biochemistry and Biophysics, vol. 300, no. 2, pp. 535–543, 1993.
[92]
Y. Yamauchi, A. Furutera, K. Seki, Y. Toyoda, K. Tanaka, and Y. Sugimoto, “Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat-stressed plants,” Plant Physiology and Biochemistry, vol. 46, no. 8-9, pp. 786–793, 2008.
[93]
I. M. M？ller and B. K. Kristensen, “Protein oxidation in plant mitochondria as a stress indicator,” Photochemical and Photobiological Sciences, vol. 3, no. 8, pp. 730–735, 2004.
[94]
M. C. Romero-Puertas, J. M. Palma, M. Gómez, L. A. Del Río, and L. M. Sandalio, “Cadmium causes the oxidative modification of proteins in pea plants,” Plant, Cell and Environment, vol. 25, no. 5, pp. 677–686, 2002.
[95]
S. J. Stohs and D. Bagchi, “Oxidative mechanisms in the toxicity of metal ions,” Free Radical Biology and Medicine, vol. 18, no. 2, pp. 321–336, 1995.
[96]
N. Brot and H. Weissbach, “The biochemistry of methionine sulfoxide residues in proteins,” Trends in Biochemical Sciences, vol. 7, no. 4, pp. 137–139, 1982.
[97]
K. J. Davies, “Protein damage and degradation by oxygen radicals. I. general aspects,” Journal of Biological Chemistry, vol. 262, no. 20, pp. 9895–9901, 1987.
[98]
P. R. Gardner and I. Fridovich, “Superoxide sensitivity of the Escherichia coli 6-phosphogluconate dehydratase,” Journal of Biological Chemistry, vol. 266, no. 3, pp. 1478–1483, 1991.
[99]
E. R. Stadtman, “Oxidation of proteins by mixed-function oxidation systems: implication in protein turnover, ageing and neutrophil function,” Trends in Biochemical Sciences, vol. 11, no. 1, pp. 11–12, 1986.
[100]
E. Cabiscol, E. Piulats, P. Echave, E. Herrero, and J. Ros, “Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae,” Journal of Biological Chemistry, vol. 275, no. 35, pp. 27393–27398, 2000.
[101]
T. Grune, T. Reinheckel, and K. J. A. Davies, “Degradation of oxidized proteins in mammalian cells,” FASEB Journal, vol. 11, no. 7, pp. 526–534, 1997.
[102]
J. A. Imlay and S. Linn, “DNA damage and oxygen radical toxicity,” Science, vol. 240, no. 4857, pp. 1302–1309, 1988.
[103]
T. Liu, J. Van Staden, and W. A. Cress, “Salinity induced nuclear and DNA degradation in meristematic cells of soybean (Glycine max (L.)) roots,” Plant Growth Regulation, vol. 30, no. 1, pp. 49–54, 2000.
[104]
M. Dizdaroglu, “Chemistry of free radical damage to DNA and nucleoproteins,” in DNA and Free Radicals, B. Halliwell and O. I. Aruoma, Eds., pp. 19–39, Ellis Horwood, London, UK, 1993.
[105]
B. Halliwell and J. M. C. Gutteridge, Free Radicals in Biology and Medicine, Oxford University Press, Oxford, UK, 3rd edition, 1999.
[106]
H. Tsuboi, K. Kouda, H. Takeuchi et al., “8-Hydroxydeoxyguanosine in urine as an index of oxidative damage to DNA in the evaluation of atopic dermatitis,” British Journal of Dermatology, vol. 138, no. 6, pp. 1033–1035, 1998.
[107]
B. Halliwell and O. I. Aruoma, “DNA damage by oxygen-derived species. Its mechanism and measurement in mammalian systems,” FEBS Letters, vol. 281, no. 1-2, pp. 9–19, 1991.
[108]
S. P. Fink, G. R. Reddy, and L. J. Marnett, “Mutagenicity in Escherichia coli of the major DNA adduct derived from the endogenous mutagen malondialdehyde,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 16, pp. 8652–8657, 1997.
[109]
M. D. Evans, M. Dizdaroglu, and M. S. Cooke, “Oxidative DNA damage and disease: induction, repair and significance,” Mutation Research, vol. 567, no. 1, pp. 1–61, 2004.
[110]
N. L. Oleinick, Song-mao Chiu, N. Ramakrishnan, and Liang-yan Xue, “The formation, identification, and significance of DNA-protein cross-links in mammalian cells,” British Journal of Cancer, supplement, vol. 8, pp. 135–140, 1987.
[111]
C. Richter, “Reactive oxygen and DNA damage in mitochondria,” Mutation Research, DNAging Genetic Instability and Aging, vol. 275, no. 3-6, pp. 249–255, 1992.
[112]
C. H. Pang and B. S. Wang, “Oxidative stress and salt tolerance in plants,” in Progress in Botany, U. Lüttge, W. Beyschlag, and J. Murata, Eds., pp. 231–245, Springer, Berlin, Germany, 2008.
[113]
P. Sharma, A. B. Jha, and R. S. Dubey, “Oxidative stress and antioxidative defense system in plants growing under abiotic Stresses,” in Handbook of Plant and Crop Stress, M. Pessarakli, Ed., pp. 89–138, CRC Press, Taylor and Francis Publishing Company, Fla, USA, 3rd edition, 2010.
[114]
M. C. De Pinto and L. De Gara, “Changes in the ascorbate metabolism of apoplastic and symplastic spaces are associated with cell differentiation,” Journal of Experimental Botany, vol. 55, no. 408, pp. 2559–2569, 2004.
[115]
Q. Gao and L. Zhang, “Ultraviolet-B-induced oxidative stress and antioxidant defense system responses in ascorbate-deficient vtc1 mutants of Arabidopsis thaliana,” Journal of Plant Physiology, vol. 165, no. 2, pp. 138–148, 2008.
[116]
N. M. Semchuk, O. V. Lushchak, J. Falk, K. Krupinska, and V. I. Lushchak, “Inactivation of genes, encoding tocopherol biosynthetic pathway enzymes, results in oxidative stress in outdoor grown Arabidopsis thaliana,” Plant Physiology and Biochemistry, vol. 47, no. 5, pp. 384–390, 2009.
[117]
G. L. Wheeler, M. A. Jones, and N. Smirnoff, “The biosynthetic pathway of vitamin C in higher plants,” Nature, vol. 393, no. 6683, pp. 365–369, 1998.
[118]
F. A. Isherwood, Y. T. Chen, and L. W. Mapson, “Synthesis of L-ascorbic acid in plants and animals,” The Biochemical Journal, vol. 56, no. 1, pp. 1–15, 1954.
[119]
H. B. Shao, L. Y. Chu, Z. H. Lu, and C. M. Kang, “Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells,” International Journal of Biological Sciences, vol. 4, no. 1, pp. 8–14, 2008.
[120]
N. Smirnoff, J. A. Running, and S. Gatzek, “Ascorbate biosynthesis: a diversity of pathways,” in Vitamin C: Its Functions and Biochemistry in Animals and Plants, H. Asard, J. M. May, and N. Smirnoff, Eds., pp. 7–29, BIOS Scientific, New York, NY, USA, 2004.
[121]
J. D. Barnes, Y. Zheng, and T. M. Lyons, “Plant resistance to ozone: the role of ascorbate,” in Air Pollution and Plant Biotechnology, K. Omasa, H. Saji, S. Youssefian, and N. Kondo, Eds., pp. 235–254, Springer, Tokyo, Japan, 2002.
[122]
N. Smirnoff, “Ascorbic acid: metabolism and functions of a multi-facetted molecule,” Current Opinion in Plant Biology, vol. 3, no. 3, pp. 229–235, 2000.
[123]
C. Miyake and K. Asada, “Ferredoxin-dependent photoreduction of the monodehydroascorbate radical in spinach thylakoids,” Plant and Cell Physiology, vol. 35, no. 4, pp. 539–549, 1994.
[124]
K. Asada, “Radical production and scavenging in the chloroplasts,” in Photosynthesis and the Environment, N. R. Baker, Ed., pp. 123–150, Kluwer, Dordrecht, The Netherlands, 1996.
[125]
J. A. Hernández, M. A. Ferrer, A. Jiménez, A. R. Barceló, and F. Sevilla, “Antioxidant systems and /H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins,” Plant Physiology, vol. 127, no. 3, pp. 817–831, 2001.
[126]
M. S. Radyuk, I. N. Domanskaya, R. A. Shcherbakov, and N. V. Shalygo, “Effect of low above-zero temperature on the content of low-molecular antioxidants and activities of antioxidant enzymes in green barley leaves,” Russian Journal of Plant Physiology, vol. 56, no. 2, pp. 175–180, 2009.
[127]
M. M. Chaves, J. S. Pereira, J. Maroco et al., “How plants cope with water stress in the field. Photosynthesis and growth,” Annals of Botany, vol. 89, pp. 907–916, 2002.
[128]
C. Zhang, J. Liu, Y. Zhang et al., “Overexpression of SlGMEs leads to ascorbate accumulation with enhanced oxidative stress, cold, and salt tolerance in tomato,” Plant Cell Reports, vol. 30, no. 3, pp. 389–398, 2011.
[129]
Hemavathi, C. P. Upadhyaya, K. E. Young et al., “Over-expression of strawberry d-galacturonic acid reductase in potato leads to accumulation of vitamin C with enhanced abiotic stress tolerance,” Plant Science, vol. 177, no. 6, pp. 659–667, 2009.
[130]
Z. Wang, Y. Xiao, W. Chen, K. Tang, and L. Zhang, “Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis,” Journal of Integrative Plant Biology, vol. 52, no. 4, pp. 400–409, 2010.
[131]
C. H. Foyer and G. Noctor, “Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria,” Physiologia Plantarum, vol. 119, no. 3, pp. 355–364, 2003.
[132]
K. Asada, “Production and action of active oxygen species in photosynthetic tissues,” in Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants, C. H. Foyer and P. M. Mullineaux, Eds., pp. 77–104, CRC Press, Boca Raton, Fla, USA, 1994.
[133]
F. A. Loewus, “Ascorbic acid and its metabolic products,” in The Biochemistry of Plants, J. Preiss, Ed., pp. 85–107, ,Academic Press, New York, NY, USA, 1988.
[134]
C. H. Foyer and B. Halliwell, “The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism,” Planta, vol. 133, no. 1, pp. 21–25, 1976.
[135]
M. Tausz, H. ？ircelj, and D. Grill, “The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid?” Journal of Experimental Botany, vol. 55, no. 404, pp. 1955–1962, 2004.
[136]
M. Hefny and D. Z. Abdel-Kader, “Antioxidant-enzyme system as selection criteria for salt tolerance in forage sorghum genotypes (Sorghum bicolor L. Moench),” in Salinity and Water Stress, M. Ashraf, M. Ozturk, and H. R. Athar, Eds., pp. 25–36, Springer, The Netherlands, 2009.
[137]
M. Strohm, M. Eiblmeier, C. Langebartels et al., “Responses of transgenic poplar (Populus tremula × P. alba) overexpressing glutathione synthetase or glutathione reductase to acute ozone stress: visible injury and leaf gas exchange,” Journal of Experimental Botany, vol. 50, no. 332, pp. 365–374, 1999.
[138]
C. H. Foyer, N. Souriau, S. Perret et al., “Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees,” Plant Physiology, vol. 109, no. 3, pp. 1047–1057, 1995.
[139]
Y. L. Zhu, E. A. H. Pilon-Smits, A. S. Tarun, S. U. Weber, L. Jouanin, and N. Terry, “Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase,” Plant Physiology, vol. 121, no. 4, pp. 1169–1177, 1999.
[140]
G. Gullner, T. K？mives, and H. Rennenberg, “Enhanced tolerance of transgenic poplar plants overexpressing γ-glutamylcysteine synthetase towards chloroacetanilide herbicides,” Journal of Experimental Botany, vol. 52, no. 358, pp. 971–979, 2001.
[141]
A. E. Eltayeb, S. Yamamoto, M. E. E. Habora et al., “Greater protection against oxidative damages imposed by various environmental stresses in transgenic potato with higher level of reduced glutathione,” Breeding Science, vol. 60, no. 2, pp. 101–109, 2010.
[142]
T. Diplock, L. J. Machlin, L. Packer, and W. A. Pryor, “Vitamin E: biochemistry and health implications,” Annals of the New York Academy of Sciences, vol. 570, pp. 372–378, 1989.
[143]
K. Fukuzawa, A. Tokumura, S. Ouchi, and H. Tsukatani, “Antioxidant activities of tocopherols on Fe2+-ascorbate-induced lipid peroxidation in lecithin liposomes,” Lipids, vol. 17, no. 7, pp. 511–514, 1982.
[144]
A. Kamal-Eldin and L. ？. Appelqvist, “The chemistry and antioxidant properties of tocopherols and tocotrienols,” Lipids, vol. 31, no. 7, pp. 671–701, 1996.
[145]
Y. Li, Y. Zhou, Z. Wang, X. Sun, and K. Tang, “Engineering tocopherol biosynthetic pathway in Arabidopsis leaves and its effect on antioxidant metabolism,” Plant Science, vol. 178, no. 3, pp. 312–320, 2010.
[146]
B. N. Ivanov and S. Khorobrykh, “Participation of photosynthetic electron transport in production and scavenging of reactive oxygen species,” Antioxidants and Redox Signaling, vol. 5, no. 1, pp. 43–53, 2003.
[147]
M. J. Fryer, “The antioxidant effect of thylakoid vitamin-E (α-tocopherol),” Plant, Cell and Environment, vol. 15, no. 4, pp. 381–392, 1992.
[148]
V. E. Kagan, J. P. Fabisiak, and P. J. Quinn, “Coenzyme Q and vitamin E need each other as antioxidants,” Protoplasma, vol. 214, no. 1-2, pp. 11–18, 2000.
[149]
K. Yamaguchi-Shinozaki and K. Shinozaki, “A novel cis element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress,” Plant Cell, vol. 6, no. 2, pp. 251–264, 1994.
[150]
S. Munné-Bosch, K. Schwarz, and L. Alegre, “Enhanced formation of α-tocopherol and highly oxidized abietane diterpenes in water-stressed rosemary plants,” Plant Physiology, vol. 121, no. 3, pp. 1047–1052, 1999.
[151]
J. Guo, X. Liu, X. Li, S. Chen, Z. Jin, and G. Liu, “Overexpression of VTE1 from Arabidopsis resulting in high vitamin E accumulation and salt stress tolerance increase in tobacco plant,” Chinese Journal of Applied and Environmental Biology, vol. 12, no. 4, pp. 468–471, 2006.
[152]
S. O. Bafeel and M. M. Ibrahim, “Antioxidants and accumulation of α-tocopherol induce chilling tolerance in Medicago sativa,” International Journal of Agriculture and Biology, vol. 10, no. 6, pp. 593–598, 2008.
[153]
S. Q. Ouyang, S. J. He, P. Liu, W. K. Zhang, J. S. Zhang, and S. Y. Chen, “The role of tocopherol cyclase in salt stress tolerance of rice (Oryza sativa),” Science China Life Sciences, vol. 54, no. 2, pp. 181–188, 2011.
[154]
J. Young, “The photoprotective role of carotenoids in higher plants,” Physiologia Plantarum, vol. 83, no. 4, pp. 702–708, 1991.
[155]
D. Sieferman-Harms, “The light harvesting function of carotenoids in photosynthetic membrane,” Plant Physiology, vol. 69, no. 3, pp. 561–568, 1987.
[156]
F. Li, R. Vallabhaneni, J. Yu, T. Rocheford, and E. T. Wurtzel, “The maize phytoene synthase gene family: overlapping roles for carotenogenesis in endosperm, photomorphogenesis, and thermal stress tolerance,” Plant Physiology, vol. 147, no. 3, pp. 1334–1346, 2008.
[157]
R. Gomathi and P. Rakkiyapan, “Comparative lipid peroxidation, leaf membrane thermostability, and antioxidant system in four sugarcane genotypes differing in salt tolerance,” International Journal of Plant Physiology and Biochemistry, vol. 3, no. 4, pp. 67–74, 2011.
[158]
S. G. Grace and B. A. Logan, “Energy dissipation and radical scavenging by the plant phenylpropanoid pathway,” Philosophical Transactions of the Royal Society B, vol. 355, no. 1402, pp. 1499–1510, 2000.
[159]
A. Arora, T. M. Byrem, M. G. Nair, and G. M. Strasburg, “Modulation of liposomal membrane fluidity by flavonoids and isoflavonoids,” Archives of Biochemistry and Biophysics, vol. 373, no. 1, pp. 102–109, 2000.
[160]
A. Michalak, “Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress,” Polish Journal of Environmental Studies, vol. 15, no. 4, pp. 523–530, 2006.
[161]
K. M. Janas, R. Amarowicz, J. Zielińska-Tomaszewska, A. Kosińska, and M. M. Posmyk, “Induction of phenolic compounds in two dark-grown lentil cultivars with different tolerance to copper ions,” Acta Physiologiae Plantarum, vol. 31, no. 3, pp. 587–595, 2009.
[162]
R. Lois and B. B. Buchanan, “Severe sensitivity to ultraviolet radiation in an Arabidopsis mutant deficient in flavonoid accumulation. II.Mechanisms of UV-resistance in Arabidopsis,” Planta, vol. 194, no. 4, pp. 504–509, 1994.
[163]
M. Lukaszewicz, I. Matysiak-Kata, J. Skala, I. Fecka, W. Cisowski, and J. Szopa, “Antioxidant capacity manipulation in transgenic potato tuber by changes in phenolic compounds content,” Journal of Agricultural and Food Chemistry, vol. 52, no. 6, pp. 1526–1533, 2004.
[164]
S. Sayfzadeh and M. Rashidi, “Response of antioxidant enzymes activities of sugar beet to drought stress,” ARPN Journal of Agricultural and Biological Science, vol. 6, no. 4, pp. 27–33, 2011.
[165]
C. Sgherri, B. Stevanovic, and F. Navari-Izzo, “Role of phenolic acids during dehydration and rehydration of Ramonda serbica,” Physiologia Plantarum, vol. 122, no. 4, pp. 478–485, 2000.
[166]
P. Mishra, B. Kumari, and R. S. Dubey, “Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive Indica rice (Oryza sativa L.) seedlings,” Protoplasma. In press.
[167]
R. Valderrama, F. J. Corpas, A. Carreras et al., “The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants,” Plant, Cell and Environment, vol. 29, no. 7, pp. 1449–1459, 2006.
[168]
R. Mittal and R. S. Dubey, “Behaviour of peroxidases in rice: changes in enzymatic activity and isoforms in relation to salt tolerance,” Plant Physiology and Biochemistry, vol. 29, no. 1, pp. 31–40, 1991.
[169]
M. J. Fryer, J. R. Andrews, K. Oxborough, D. A. Blowers, and N. R. Baker, “Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature,” Plant Physiology, vol. 116, no. 2, pp. 571–580, 1998.
[170]
Y. Zhang, Y. Luo, Y. X. Hou, H. Jiang, Q. Chen, and R. H. Tang, “Chilling acclimation induced changes in the distribution of H2O2 and antioxidant system of strawberry leaves,” Agricultural Journal, vol. 3, no. 4, pp. 286–291, 2008.
[171]
I. Cakmak and W. J. Horst, “Effect of aluminium on lipid peroxidation, superoxide dismuatse, catalase, and peroxidase activities in root tips of soybean (Glycine max),” Physiologia Plantarum, vol. 83, no. 3, pp. 463–468, 1991.
[172]
M. V. Rao, G. Paliyath, and D. P. Ormrod, “Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana,” Plant Physiology, vol. 110, no. 1, pp. 125–136, 1996.
[173]
N. A. Ashry and H. I. Mohamed, “Impact of secondary metabolites and related enzymes in flax resistance and/or susceptibility to powdery mildew,” African Journal of Biotechnology, vol. 11, no. 5, pp. 1073–1077, 2012.
[174]
D. E. M. Radwan, K. A. Fayez, S. Y. Mahmoud, and G. Lu, “Modifications of antioxidant activity and protein composition of bean leaf due to Bean yellow mosaic virus infection and salicylic acid treatments,” Acta Physiologiae Plantarum, vol. 32, no. 5, pp. 891–904, 2010.
[175]
J. G. Scandalios, “Oxygen stress and superoxide dismutases,” Plant Physiology, vol. 101, no. 1, pp. 7–12, 1993.
[176]
I. Fridovich, “Superoxide dismutases. An adaptation to a paramagnetic gas,” Journal of Biological Chemistry, vol. 264, no. 14, pp. 7761–7764, 1989.
[177]
M. L. Racchi, F. Bagnoli, I. Balla, and S. Danti, “Differential activity of catalase and superoxide dismutase in seedlings and in vitro micropropagated oak (Quercus robur L.),” Plant Cell Reports, vol. 20, no. 2, pp. 169–174, 2001.
[178]
C. Bowler, M. Van Montagu, and D. Inzé, “Superoxide dismutase and stress tolerance,” Annual Review of Plant Physiology and Plant Molecular Biology, vol. 43, no. 1, pp. 83–116, 1992.
[179]
C. Jackson, J. Dench, A. L. Moore, B. Halliwell, C. H. Foyer, and D. O. Hall, “Subcellular localisation and identification of superoxide dismutase in the leaves of higher plants,” European Journal of Biochemistry, vol. 91, no. 2, pp. 339–344, 1978.
[180]
S. Kanematsu and K. Asada, “Cuzn-superoxide dismutases in rice: occurrence of an active, monomeric enzyme and two types of isozyme in leaf and non-photosynthetic tissues,” Plant and Cell Physiology, vol. 30, no. 3, pp. 381–391, 1989.
[181]
P. Bueno, J. Varela, G. Gimenez-Gallego, and L. A. Del Rio, “Peroxisomal copper, zinc superoxide dismutase. Characterization of the isoenzyme from watermelon cotyledons,” Plant Physiology, vol. 108, no. 3, pp. 1151–1160, 1995.
[182]
L. A. Del Río, G. M. Pastori, J. M. Palma et al., “The activated oxygen role of peroxisomes in senescence,” Plant Physiology, vol. 116, no. 4, pp. 1195–1200, 1998.
[183]
A. S. Gupta, J. L. Heinen, A. S. Holaday, J. J. Burke, and R. D. Allen, “Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 4, pp. 1629–1633, 1993.
[184]
G. Scandalios, L. Guan, and A. N. Polidoros, “Catalases in plants: gene structure, properties, regulation and expression,” in Oxidative Stress and the Molecular Biology of Antioxidants Defenses, J. G. Scandalios, Ed., pp. 343–406, Cold Spring Harbor Laboratory Press, New York, NY, USA, 1997.
[185]
F. J. Corpas, J. M. Palma, L. M. Sandalio, R. Valderrama, J. B. Barroso, and L. A. del Río, “Peroxisomal xanthine oxidoreductase: characterization of the enzyme from pea (Pisum sativum L.) leaves,” Journal of Plant Physiology, vol. 165, no. 13, pp. 1319–1330, 2008.
[186]
A. Mhamdi, G. Queval, S. Chaouch, S. Vanderauwera, F. Van Breusegem, and G. Noctor, “Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models,” Journal of Experimental Botany, vol. 61, no. 15, pp. 4197–4220, 2010.
[187]
H. Willekens, D. Inze, M. Van Montagu, and W. Van Camp, “Catalases in plants,” Molecular Breeding, vol. 1, no. 3, pp. 207–228, 1995.
[188]
N. Mallick and F. H. Mohn, “Reactive oxygen species: response of algal cells,” Journal of Plant Physiology, vol. 157, no. 2, pp. 183–193, 2000.
[189]
R. Moussa and S. M Abdel-Aziz, “Comparative response of drought tolerant and drought sensitive maize genotypes to water stress,” Australian Journal of Crop Sciences, vol. 1, no. 1, pp. 31–36, 2008.
[190]
H. Willekens, S. Chamnongpol, M. Davey et al., “Catalase is a sink for H2O2 and is indispensable for stress defence in C-3 plants,” EMBO Journal, vol. 16, no. 16, pp. 4806–4816, 1997.
[191]
Z. Guan, T. Chai, Y. Zhang, J. Xu, and W. Wei, “Enhancement of Cd tolerance in transgenic tobacco plants overexpressing a Cd-induced catalase cDNA,” Chemosphere, vol. 76, no. 5, pp. 623–630, 2009.
[192]
D. J. Schuller, N. Ban, R. B. Van Huystee, A. McPherson, and T. L. Poulos, “The crystal structure of peanut peroxidase,” Structure, vol. 4, no. 3, pp. 311–321, 1996.
[193]
K. Asada, “Ascorbate peroxidase: a hydrogen peroxide scavenging enzyme in plants,” Physiologia Plantarum, vol. 85, no. 2, pp. 235–241, 1992.
[194]
K. Kobayashi, Y. Kumazawa, K. Miwa, and S. Yamanaka, “ε-(γ-Glutamyl)lysine cross-links of spore coat proteins and transglutaminase activity in Bacillus subtilis,” FEMS Microbiology Letters, vol. 144, no. 2-3, pp. 157–160, 1996.
[195]
J. Vangronsveld and H. Clijsters, “Toxic effects of metals,” in Plants and the Chemical Elements. Biochemistry, Uptake, Tolerance and Toxicity, M. E. Farago, Ed., pp. 150–177, VCH Publishers, Weinheim, Germany, 1994.
[196]
K. Radoti？, T. Du？i？, and D. Mutavd？i？, “Changes in peroxidase activity and isoenzymes in spruce needles after exposure to different concentrations of cadmium,” Environmental and Experimental Botany, vol. 44, no. 2, pp. 105–113, 2000.
[197]
H. Tayefi-Nasrabadi, G. Dehghan, B. Daeihassani, A. Movafegi, and A. Samadi, “Some biochemical properties of guaiacol peroxidases as modified by salt stress in leaves of salt-tolerant and salt-sensitive safflower (Carthamus tinctorius L.cv.) cultivars,” African Journal of Biotechnology, vol. 10, no. 5, pp. 751–763, 2011.
[198]
A. Jiménez, J. A. Hernández, L. A. Del Río, and F. Sevilla, “Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves,” Plant Physiology, vol. 114, no. 1, pp. 275–284, 1997.
[199]
J. E. Pallanca and N. Smirnoff, “The control of ascorbic acid synthesis and turnover pea seedlings,” Journal of Experimental Botany, vol. 51, no. 345, pp. 669–674, 2000.
[200]
K. G. Welinder, “Superfamily of plant, fungal and bacterial peroxidases,” Current Opinion in Structural Biology, vol. 2, no. 3, pp. 388–393, 1992.
[201]
W. R. Patterson and T. L. Poulos, “Crystal structure of recombinant pea cytosolic ascorbate peroxidase,” Biochemistry, vol. 34, no. 13, pp. 4331–4341, 1995.
[202]
R. Madhusudhan, T. Ishikawa, Y. Sawa, S. Shigeoka, and H. Shibata, “Characterization of an ascorbate peroxidase in plastids of tobacco BY-2 cells,” Physiologia Plantarum, vol. 117, no. 4, pp. 550–557, 2003.
[203]
P. Sharma and R. S. Dubey, “Ascorbate peroxidase from rice seedlings: properties of enzyme isoforms, effects of stresses and protective roles of osmolytes,” Plant Science, vol. 167, no. 3, pp. 541–550, 2004.
[204]
Y. Nakano and K. Asada, “Purification of ascorbate peroxidase in spinach chloroplasts; its inactivation in ascorbate-depleted medium and reactivation by monodehydroascorbate radical,” Plant and Cell Physiology, vol. 28, no. 1, pp. 131–140, 1987.
[205]
R. Mittler and B. A. Zilinskas, “Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase,” Journal of Biological Chemistry, vol. 267, no. 30, pp. 21802–21807, 1992.
[206]
T. Ishikawa, K. Yoshimura, K. Sakai, M. Tamoi, T. Takeda, and S. Shigeoka, “Molecular characterization and physiological role of a glyoxysome-bound ascorbate peroxidase from spinach,” Plant and Cell Physiology, vol. 39, no. 1, pp. 23–34, 1998.
[207]
J. Wang, H. Zhang, and R. D. Allen, “Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress,” Plant and Cell Physiology, vol. 40, no. 7, pp. 725–732, 1999.
[208]
Y. C. Boo and J. Jung, “Water deficit - Induced oxidative stress and antioxidative defenses in rice plants,” Journal of Plant Physiology, vol. 155, no. 2, pp. 255–261, 1999.
[209]
Y. Wang, M. Wisniewski, R. Meilan, M. Cui, R. Webb, and L. Fuchigami, “Overexpression of cytosolic ascorbate peroxidase in tomato confers tolerance to chilling and salt stress,” Journal of the American Society for Horticultural Science, vol. 130, no. 2, pp. 167–173, 2005.
[210]
Y. Yabuta, T. Motoki, K. Yoshimura, T. Takeda, T. Ishikawa, and S. Shigeoka, “Thylakoid membrane-bound ascorbate peroxidase is a limiting factor of antioxidative systems under photo-oxidative stress,” Plant Journal, vol. 32, no. 6, pp. 915–925, 2002.
[211]
T. Ushimaru, Y. Maki, S. Sano, K. Koshiba, K. Asada, and H. Tsuji, “Induction of Enzymes Involved in the Ascorbate-Dependent Antioxidative System, Namely, Ascorbate Peroxidase, Monodehydroascorbate Reductase and Dehydroascorbate Reductase, after Exposure to Air of Rice (Oryza sativa) Seedlings Germinated under Water,” Plant and Cell Physiology, vol. 38, no. 5, pp. 541–549, 1997.
[212]
M. A. Hossain and K. Asada, “Monodehydroascorbate reductase from cucumber is a flavin adenine dinucleotide enzyme,” Journal of Biological Chemistry, vol. 260, no. 24, pp. 12920–12926, 1985.
[213]
Y. Sakihama, J. Mano, S. Sano, K. Asada, and H. Yamasaki, “Reduction of phenoxyl radicals mediated by monodehydroascorbate reductase,” Biochemical and Biophysical Research Communications, vol. 279, no. 3, pp. 949–954, 2000.
[214]
M. A. Hossain, Y. Nakano, and K. Asada, “Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide,” Plant and Cell Physiology, vol. 25, no. 3, pp. 385–395, 1984.
[215]
D. A. Dalton, L. M. Baird, L. Langeberg et al., “Subcellular localization of oxygen defense enzymes in soybean (Glycine max [L.] Merr.) root nodules,” Plant Physiology, vol. 102, no. 2, pp. 481–489, 1993.
[216]
C. Miyake, U. Schreiber, H. Hormann, S. Sano, and K. Asada, “The FAD-enzyme monodehydroascorbate radical reductase mediates photoproduction of superoxide radicals in spinach thylakoid membranes,” Plant and Cell Physiology, vol. 39, no. 8, pp. 821–829, 1998.
[217]
A. E. Eltayeb, N. Kawano, G. H. Badawi et al., “Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses,” Planta, vol. 225, no. 5, pp. 1255–1264, 2007.
[218]
F. Li, Q. Y. Wu, Y. L. Sun, L. Y. Wang, X. H. Yang, and Q. W. Meng, “Overexpression of chloroplastic monodehydroascorbate reductase enhanced tolerance to temperature and methyl viologen-mediated oxidative stresses,” Physiologia Plantarum, vol. 139, no. 4, pp. 421–434, 2010.
[219]
Z. Chen, T. E. Young, J. Ling, S. C. Chang, and D. R. Gallie, “Increasing vitamin C content of plants through enhanced ascorbate recycling,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 6, pp. 3525–3530, 2003.
[220]
A. Qin, Q. Shi, and X. Yu, “Ascorbic acid contents in transgenic potato plants overexpressing two dehydroascorbate reductase genes,” Molecular Biology Reports, vol. 38, no. 3, pp. 1557–1566, 2011.
[221]
M. A. Hossain and K. Asada, “Purification of dehydroascorbate reductase from spinach and its characterization as a thiol enzyme,” Plant and Cell Physiology, vol. 25, no. 1, pp. 85–92, 1984.
[222]
S. Dipierro and G. Borraccino, “Dehydroascorbate reductase from potato tubers,” Phytochemistry, vol. 30, no. 2, pp. 427–429, 1991.
[223]
S. Yoshida, M. Tamaoki, T. Shikano et al., “Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana,” Plant and Cell Physiology, vol. 47, no. 2, pp. 304–308, 2006.
[224]
M. C. Rubio, P. Bustos-Sanmamed, M. R. Clemente, and M. Becana, “Effects of salt stress on the expression of antioxidant genes and proteins in the model legume Lotus japonicus,” New Phytologist, vol. 181, no. 4, pp. 851–859, 2009.
[225]
A. E. Eltayeb, S. Yamamoto, M. E.E. Habora, L. Yin, H. Tsujimoto, and K. Tanaka, “Transgenic potato overexpressing Arabidopsis cytosolic AtDHAR1 showed higher tolerance to herbicide, drought and salt stresses,” Breeding Science, vol. 61, no. 1, pp. 3–10, 2011.
[226]
S. Ghisla and V. Massey, “Mechanisms of flavoprotein-catalyzed reactions,” European Journal of Biochemistry, vol. 181, no. 1, pp. 1–17, 1989.
[227]
E. A. Edwards, S. Rawsthorne, and P. M. Mullineaux, “Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.),” Planta, vol. 180, no. 2, pp. 278–284, 1990.
[228]
G. M. Pastori and V. S. Trippi, “Oxidative stress induces high rate of glutathione reductase synthesis in a drought-resistant maize strain,” Plant and Cell Physiology, vol. 33, no. 7, pp. 957–961, 1992.
[229]
D. -F. Shu, L. -Y. Wang, M. Duan, Y. -S. Deng, and Q. -W. Meng, “Antisense-mediated depletion of tomato chloroplast glutathione reductase enhances susceptibility to chilling stress,” Plant Physiology and Biochemistry, vol. 49, no. 10, pp. 1228–1237, 2011.
[230]
M. Aono, A. Kubo, H. Saji, K. Tanaka, and N. Kondo, “Enhanced tolerance to photooxidative stress of transgenic Nicotiana tabacum with high chloroplastic glutathione reductase activity,” Plant and Cell Physiology, vol. 34, no. 1, pp. 129–135, 1993.
[231]
M. J. Tseng, C. W. Liu, and J. C. Yiu, “Tolerance to sulfur dioxide in transgenic Chinese cabbage transformed with both the superoxide dismutase containing manganese and catalase genes of Escherichia coli,” Scientia Horticulturae, vol. 115, no. 2, pp. 101–110, 2008.
[232]
S. C. Lee, S. Y. Kwon, and S. R. Kim, “Ectopic expression of a cold-responsive CuZn superoxide dismutase gene, SodCc1, in transgenic rice (Oryza sativa L.),” Journal of Plant Biology, vol. 52, no. 2, pp. 154–160, 2009.
[233]
M. Aono, H. Saji, A. Sakamoto, K. Tanaka, N. Kondo, and Tanaka, “Paraquat tolerance of transgenic Nicotiana tabacum with enhanced activities of glutathione reductase and superoxide dismutase,” Plant and Cell Physiology, vol. 36, no. 8, pp. 1687–1691, 1995.
[234]
S. Y. Kwon, Y. J. Jeong, H. S. Lee et al., “Enhanced tolerances of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress,” Plant, Cell and Environment, vol. 25, no. 7, pp. 873–882, 2002.
[235]
S. Lim, Y. H. Kim, S. H. Kim et al., “Enhanced tolerance of transgenic sweetpotato plants that express both CuZnSOD and APX in chloroplasts to methyl viologen-mediated oxidative stress and chilling,” Molecular Breeding, vol. 19, no. 3, pp. 227–239, 2007.
[236]
S. S. Kwak, S. Lim, L. Tang, S. Y. Kwon, and H. S. Lee, “Enhanced tolerance of transgenic crops expressing both SOD and APX in chloroplasts to multiple environmental stress,” in Salinity and Water Stress, M. Ashraf, M. Ozturk, and H. R. Athar, Eds., pp. 197–203, Springer, Netherland, 2009.
[237]
K. Asada, “The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons,” Annual Review of Plant Biology, vol. 50, pp. 601–639, 1999.
[238]
K. Biehler and H. Fock, “Evidence for the contribution of the Mehler-peroxidase reaction in dissipating excess electrons in drought-stressed wheat,” Plant Physiology, vol. 112, no. 1, pp. 265–272, 1996.
[239]
C. H. Foyer and G. Noctor, “Oxygen processing in photosynthesis: regulation and signalling,” New Phytologist, vol. 146, no. 3, pp. 359–388, 2000.
[240]
R. K. Sairam, P. S. Deshmukh, and D. C. Saxena, “Role of antioxidant systems in wheat genotypes tolerance to water stress,” Biologia Plantarum, vol. 41, no. 3, pp. 387–394, 1998.
[241]
S. Wang, D. Liang, C. Li, Y. Hao, F. Ma, and H. Shu, “Influence of drought stress on the cellular ultrastructure and antioxidant system in leaves of drought-tolerant and drought-sensitive apple rootstocks,” Plant Physiology and Biochemistry, vol. 51, pp. 81–89, 2012.
[242]
J. A. Hernández, A. Jiménez, P. Mullineaux, and F. Sevilla, “Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences,” Plant, Cell and Environment, vol. 23, no. 8, pp. 853–862, 2000.
[243]
U. Perez-Lopez, A. Robredo, M. Lacuesta et al., “The oxidative stress caused by salinity in two barley cultivars is mitigated by elevated CO2,” Physiologia Plantarum, vol. 135, no. 1, pp. 29–42, 2009.
[244]
N. Karray-Bouraoui, F. Harbaoui, M. Rabhi et al., “Different antioxidant responses to salt stress in two different provenances of Carthamus tinctorius L,” Acta Physiologiae Plantarum, vol. 33, no. 4, pp. 1435–1444, 2011.
[245]
X. Wang, P. Yang, Q. Gao et al., “Proteomic analysis of the response to high-salinity stress in Physcomitrella patens,” Planta, vol. 228, no. 1, pp. 167–177, 2008.
[246]
H. Vaidyanathan, P. Sivakumar, R. Chakrabarty, and G. Thomas, “Scavenging of reactive oxygen species in NaCl-stressed rice (Oryza sativa L.) - Differential response in salt-tolerant and sensitive varieties,” Plant Science, vol. 165, no. 6, pp. 1411–1418, 2003.
[247]
A. Shalata, V. Mittova, M. Volokita, M. Guy, and M. Tal, “Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: the root antioxidative system,” Physiologia Plantarum, vol. 112, no. 4, pp. 487–494, 2001.
[248]
A. Hediye Sekmen, I. Türkan, and S. Takio, “Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media,” Physiologia Plantarum, vol. 131, no. 3, pp. 399–411, 2007.
[249]
B. A. Logan, D. Kornyeyev, J. Hardison, and A. S. Holaday, “The role of antioxidant enzymes in photoprotection,” Photosynthesis Research, vol. 88, no. 2, pp. 119–132, 2006.
[250]
Y. H. Zhou, J. Q. Yu, W. H. Mao, L. F. Huang, X. S. Song, and S. Nogués, “Genotypic variation of Rubisco expression, photosynthetic electron flow and antioxidant metabolism in the chloroplasts of chill-exposed cucumber plants,” Plant and Cell Physiology, vol. 47, no. 2, pp. 192–199, 2006.
[251]
T. K. Prasad, “Role of catalase in inducing chilling tolerance in pre-emergent maize seedlings,” Plant Physiology, vol. 114, no. 4, pp. 1369–1376, 1997.
[252]
Y. Zhang, H. R. Tang, and Y. Luo, “Variation in antioxidant enzyme activities of two strawberry cultivars with short-term low temperature stress,” World Journal of Agricultural Sciences, vol. 4, no. 4, pp. 458–462, 2008.
[253]
L. S. Jahnke, M. R. Hull, and S. P. Long, “Chilling stress and oxygen metabolizing enzymes in Zea mays and Zea diploperennis,” Plant, Cell and Environment, vol. 14, no. 1, pp. 97–104, 1991.
[254]
D. M. Hodges, C. J. Andrews, D. A. Johnson, and R. I. Hamilton, “Antioxidant compound responses to chilling stress in differentially sensitive inbred maize lines,” Physiologia Plantarum, vol. 98, no. 4, pp. 685–692, 1996.
[255]
M. Huang and Z. Guo, “Responses of antioxidative system to chilling stress in two rice cultivars differing in sensitivity,” Biologia Plantarum, vol. 49, no. 1, pp. 81–84, 2005.
[256]
D. E. Salt, M. Blaylock, N. P. B. A. Kumar et al., “Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants,” Biotechnology, vol. 13, no. 5, pp. 468–474, 1995.
[257]
S. Mishra and R. S. Dubey, “Heavy metal toxicity induced alterations in photosynthetic metabolism in plants,” in Handbook of Photosynthesis, M. Pessarakli, Ed., pp. 845–863, CRC Press, Taylor and Francis Publishing Company, Fla, USA, 2nd edition, 2005.
[258]
S. Gallego, M. Benavides, and M. Tomaro, “Involvement of an antioxidant defence system in the adaptive response to heavy metal ions in Helianthus annuus L. cells,” Plant Growth Regulation, vol. 36, no. 3, pp. 267–273, 2002.
[259]
F. Vinit-Dunand, D. Epron, B. Alaoui-Sossé, and P. M. Badot, “Effects of copper on growth and on photosynthesis of mature and expanding leaves in cucumber plants,” Plant Science, vol. 163, no. 1, pp. 53–58, 2002.
[260]
M. Moustakas, T. Lanaras, L. Symeonidis, and S. Karataglis, “Growth and some photosynthetic characteristics of field grown Avena sativa under copper and lead stress,” Photosynthetica, vol. 30, no. 3, pp. 389–396, 1994.
[261]
A. ？róbek-Sokolnik, H. Asard, K. Górska-Koplińska, and R. J. Górecki, “Cadmium and zinc-mediated oxidative burst in tobacco BY-2 cell suspension cultures,” Acta Physiologiae Plantarum, vol. 31, no. 1, pp. 43–49, 2009.
[262]
S. M. Gallego, M. P. Benavides, and M. L. Tomaro, “Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress,” Plant Science, vol. 121, no. 2, pp. 151–159, 1996.
[263]
J. E. J. Weckx and H. M. M. Clijsters, “Oxidative damage and defense mechanisms in primary leaves of Phaseolus vulgaris as a result of root assimilation of toxic amounts of copper,” Physiologia Plantarum, vol. 96, no. 3, pp. 506–512, 1996.
[264]
Y. Yamamoto, A. Hachiya, and H. Matsumoto, “Oxidative damage to membranes by a combination of aluminum and iron in suspension-cultured tobacco cells,” Plant and Cell Physiology, vol. 38, no. 12, pp. 1333–1339, 1997.
[265]
S. S. Sharma and K. J. Dietz, “The relationship between metal toxicity and cellular redox imbalance,” Trends in Plant Science, vol. 14, no. 1, pp. 43–50, 2009.
[266]
L. M. Sandalio, M. Rodríguez-Serrano, L. A. del Río, and M. C. Romero-Puertas, “Reactive oxygen species and signaling in cadmium toxicity,” in Reactive Oxygen Species in Plant Signaling, L. A. Rio and A. Puppo, Eds., pp. 175–189, Springer, Berlin, Germany, 2009.
[267]
A. Giannakoula, M. Moustakas, T. Syros, and T. Yupsanis, “Aluminum stress induces up-regulation of an efficient antioxidant system in the Al-tolerant maize line but not in the Al-sensitive line,” Environmental and Experimental Botany, vol. 67, no. 3, pp. 487–494, 2010.
[268]
S. Srivastava, A. K. Srivastava, P. Suprasanna, and S. F. D'souza, “Comparative antioxidant profiling of tolerant and sensitive varieties of Brassica juncea L. to arsenate and arsenite exposure,” Bulletin of Environmental Contamination and Toxicology, vol. 84, no. 3, pp. 342–346, 2010.
[269]
M. Blumthaler and W. Ambach, “Indication of increasing solar ultraviolet-B radiation flux in alpine regions,” Science, vol. 248, no. 4952, pp. 206–208, 1990.
[270]
D. J. Allen, I. F. Mckee, P. K. Farage, and N. R. Baker, “Analysis of limitations to CO2 assimilation on exposure of leaves of two Brassica napus cultivars to UV-B,” Plant, Cell and Environment, vol. 20, no. 5, pp. 633–640, 1997.
[271]
J. He, L. K. Huang, W. S. Chow, M. L. Whitecross, and J. M Anderson, “Effects of supplementary ultraviolet-B radiation on rice and pea plants,” Australian Journal of Plant Physiology, vol. 20, no. 2, pp. 129–142, 1993.
[272]
A. Strid, W. S. Chow, and J. M. Anderson, “UV-B damage and protection at the molecular level in plants,” Photosynthesis Research, vol. 39, no. 3, pp. 475–489, 1994.
[273]
N. Doke, “Generation of superoxide anion by potato tuber protoplasts during the hypersensitive response to hyphal wall components of Phytophthora infestans and specific inhibition of the reaction by suppressors of hypersensitivity,” Physiological Plant Pathology, vol. 23, no. 3, pp. 359–367, 1983.
[274]
J. J. Grant, B. W. Yun, and G. J. Loake, “Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity,” Plant Journal, vol. 24, no. 5, pp. 569–582, 2000.
[275]
J. M. Chittoor, J. E. Leach, and F. F. White, “Differential induction of a peroxidase gene family during infection of rice by Xanthomonas oryzae pv. oryzae,” Molecular Plant-Microbe Interactions, vol. 10, no. 7, pp. 861–871, 1997.
[276]
K. Sasaki, T. Iwai, S. Hiraga et al., “Ten rice peroxidases redundantly respond to multiple stresses including infection with rice blast fungus,” Plant and Cell Physiology, vol. 45, no. 10, pp. 1442–1452, 2004.
[277]
H. Abdollahi and Z. Ghahremani, “The role of chloroplasts in the interaction between Erwinia amylovora and host plants,” Acta Horticulturae, vol. 896, pp. 215–221, 2011.
[278]
Y. Liu, D. Ren, S. Pike, S. Pallardy, W. Gassmann, and S. Zhang, “Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade,” Plant Journal, vol. 51, no. 6, pp. 941–954, 2007.
[279]
R. Mittler, E. H. Herr, B. L. Orvar et al., “Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 24, pp. 14165–14170, 1999.
