Importance of Reactive Oxygen Species in Plants-Pathogens Interactions

Yıl 2014, Cilt: 28 Sayı: 1, 11 - 21, 15.09.2015

Kubilay Baştaş

Öz

Plant pathogens have developed various independent and well-elaborated mechanisms of penetrating and accessing plant cell contents. The production of reactive oxygen species (ROS) by the consumption of molecular oxygen during host–pathogen interactions is termed the oxidative burst. The most important ROS are singlet oxygen, the hydroxyperoxyl radical, the superoxide anion, hydrogen peroxide, the hydroxyl radical and the closely related reactive nitrogen species, nitric oxide. There are profound differences between monocots and dicots as well as in the biology of biotrophic, hemibiotrophic and necrotrophic pathogens. ROS acts synergistically in a signal amplification to drive the hypersensitive reaction (HR) and the establishment of systemic defenses. The role of ROS in successful pathogenesis, it is important to try to inhibit the cell death machinery selectively and simultaneously to monitor other defense and pathogenesis-related events. With the understanding of the molecular mechanisms underlying the localized activation of the oxidative burst following perception of pathogen avirulence signals and key downstream responses including gene activation, cell death, and long-distance signaling, novel strategies will be developed for engineering enhanced protection against pathogens by manipulation of the oxidative burst and oxidant-mediated signal pathways. In this review, it is assessed the different roles of ROS in host–pathogen interactions with special emphasis on plant pathogens.

Anahtar Kelimeler

ROS, plant, pathogen, molecular interaction, defense, pathogenesis, oxidative burst

Kaynakça

• Abdollahi H, Ghahremani Z (2011). “The role of chloroplasts in the interaction between Erwinia amylovora and host plants,” Acta Horticulturae (ISHS), vol. 896, pp. 215-221,
• Aist J R, Brushnell W R (1991). Invasion of plants by powdery mildew fungi, and cellular mechanisms of resistance; in: The fungal spore and disease interaction in plants and animals (eds) G T Cole and H C Hoch (New York: Plenum Press) pp 321–345
• Albert FG, Benet LW & Anderson AJ (1986). Peroxidase associated with the root surface of Phaseols vulgaris. Can J Bot 64: 573–578.
• Alfano JR, Bauer DW, Milos TM Collmer A (1996). A. Analysis of the role of the Pseudomonas syringae pv. syringae HrpZ harpin in elicitation of the hypersensitive response in tobacco using functionally non-polar hrpZ deletion mutations, truncated HrpZ fragments, and hrmA mutations. Mol. Microbiol. 19, 715–728.
• Ali R, Ma W, Lemtiri-Chlieh, F, Tsaltas, D, Leng, Q, von Bodman, S., et al. (2007). Death don't have no mercy and neither does calcium: Arabidopsis Cyclic Nucleotide Gated Channel 2 and innate immunity. The Plant Cell, 19, 1081–1095.
• Allan AC, Lapidot M, Culver JN, Fluhr R (2001). An early tobacco mosaic virus-induced oxidative burst in tobacco indicates extracellular perception of the virus coat protein. Plant Physiol 126: 97–108
• Asada K (1999). The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:601–39
• Asada K, Takahashi M (1987). “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, 9th edition,
• Baker C J, Orlandi E W (1995). Active oxygen in plant pathogenesis. Annual Review of Phytopathology, 33, 299– 321.
• Bender CL, Stone HE, Sims JJ & Cooksey DA (1987). Reduced pathogen fitness of Pseudomonas syringae pv. tomato Tn5 mutants defective in coronatine production. Physiol Mol Plant Pathol 30: 272–283.
• Bindschedler L, V, Dewdney, J, Blee, K. A., Stone, J. M., Asai, T., Plotnikov, J., et al. (2006). Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. The Plant Journal, 47, 851–863.
• Bolwell GP, Wojtaszek P (1997). Mechanisms for the generation of reactive oxygen species in plant defence – a broad perspective. Physiol Mol Plant Pathol 51: 347 – 366
• Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F (2002). The apoplastic oxidative burst in elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 1992, 257, 85–88.
• Bolwell GP, Davies DR, Gerrish C, Auh CK, Murphy TM (1998). Comparative biochemistry of the oxidative burst produced by rose and French bean cells reveals two distinct mechanisms. Plant Physiol 116: 1379–1385.
• Borsani O, Valpuesta V and Botella M A (2003). Developing salt tolerance plants in a new century: a molecular biology approach; Plant Cell Tissue Organ Cult. 73 101–115
• Bradley D, Kjellbom P, Lamb C (1992). Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70: 21–30.
• Britto D T, Kronzucker H J (2001). Can unidirectional influx be measured in higher plants? A mathematical approach using parameters from efflux analysis; New Phytol. 150 37–47
• Brown I, Trethowan J, Kerry M, Mansfield J and Bolwell G P (1998). Localization of components of the oxidative cross-linking of glycoproteins and of callose synthesis in papillae formed duringthe interaction bet ween non-pathogenic strains of Xanthomonas campestris and French bean mesophyll cells; Plant J. 15 333–343.
• Buell RC, Joardar V, Lindeberg M et al. (2003). The complete genome of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. P Natl Acad Sci USA 100: 10181–10186.
• Catherine Gapper and Liam Dolan(2006). Control of Plant Development by Reactive Oxygen Species. Plant Physiology, June Vol. 141, pp. 341–345
• Chamnongpol S, Willekens H, Moeder W, Langebartels C, Sanderman HJ, Van Montagu M, Inze D, Van Camp W (1998). Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco. Proc Natl Acad Sci USA 95: 5818–5823
• Chang W-S, van de Mortel M, Nielsen L, de Guzman GN, Li X & Halverson LJ (2007). Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J Bacteriol 189: 8290–8299.
• Chisholm, S. T, Coaker G, Day B & Staskawicz, B. J. (2006). Host–microbe interactions: Shaping the evolution of the plant immune response. Cell, 124, 803–814.
• Chittoor J. M. 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.
• Clarke SF, Guy PL, Burritt DJ, Jameson PE (2002). Changes in the activities of antioxidant enzymes in response to virus infection and hormone treatment. Physiol Plant 114: 157–164
• Costet L, Dorey S, Fritig B, Kauffmann S (2002). A pharmacological approach to test the diffusible signal activity of reactive oxygen intermediates in elicitor-treated tobacco leaves. Plant Cell Physiol 43: 91–98
• Dat JF, Pellinen R, Beeckman T, Van De Cotte B, Langebartels C, Kangasjarvi J, Inze D, Van Breusegem F (2003). Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Plant J 33: 621–632
• Desikan R, Hancock JT, Coffey MJ, Neill SJ. (1996). Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme. FEBS Lett. 382:213–17
• Desikan, R, S. A. H. Mackerness, J. T. Hancock, and S. J. Neill ( 2001). “Regulation of the Arabidopsis transcriptome by oxidative stress,” Plant Physiology, vol. 127, no. 1, pp. 159-172
• Doke N and Miura Y (1995). In vitro activation of NADPHdependent O2 – generating system in a plasma membrane-rich fraction of potato tuber tissues by treatment with an elicitor from Phytophthora infestans or with digitonin; Physiol. Mol. Plant Pathol. 46 17–28
• Dorey S, Baillieul F, Saindrenan P, Fritig B, Kauffmann S (1998). Tobacco class I and II catalases are differentially expressed during elicitorinduced hypersensitive cell death and localized acquired resistance. Mol Plant Microbe Interact 11: 1102–1109
• Dorey S, Kopp M, Geoffroy P, Fritig B, Kauffmann S (1999). Hydrogen peroxide from the oxidative burst is neither necessary nor sufficient for hypersensitive cell death induction, phenylalanine ammonia lyase stimulation, salicylic acid accumulation or scopoletin consumption in cultured tobacco cells treated with elicitor. Plant Physiol 121: 163–173
• Draper J (1997). Salicylate, superoxide synthesis and cell suicide in plant defense. Trends Plant Sci 2: 162–165
• Durrant WE, Dong X (2004). Systemic acquired resistance. Annu Rev Phytopathol 42: 185–209
• Ferreira R. B., Monteiro, S., Freitas, R., Santos, C. N., Chen, Z .,Batista, L. M., et al. (2007). The role of plant defence proteins in fungal pathogenesis. Molecular Plant Pathology, 8, 677–700.
• Finn RD, Mistry J, Tate J et al. (2010). The Pfam protein families database. Nucleic Acids Res 38: D211–D222.
• Fones H, Preston G M (2012). Reactive oxygen and oxidative stress tolerance in plant pathogenic Pseudomonas. FEMS Microbiol Lett 327 1–8.
• Foyer C. H. and J. Harbinson(1994). “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
• Gao Q. and L. Zhang(2008). “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
• Glazner, J. A., Orlandi, E. W., & Baker, C. J. (1996). The active oxygen response of cell suspensions to incompatible bacteria is not sufficient to cause hypersensitive cell death. Plant Physiology, 110, 759–763.
• Gomez-Gomez L , Boller T (2002). Flagellin perception: a paradigm for innate immunity . Trends Plant Sci 7 : 251 – 256
• Govrin E, Levine A (2000). The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10: 751–757
• Grant JJ, Yun B-W, Loake GJ (2000a). 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 J 24: 569–582
• Grant M, Brown I,Adams S, KnightM, AinslieA, Mansfield J (2000b). The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23: 441–450
• Grant SR, Fisher EJ, Chang JH, Mole BM & Dangl JL (2006). Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu Rev Microbiol 60: 425–449.
• Grant J, Yun B. W, Loake G J ( 2000). “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,” The Plant Journal, vol. 24, no. 5, pp. 569-582
• Greenberg J. T (1997). Programmed cell death in plant– pathogen interactions. Annual Review of Plant Physiology and Plant Molecular Biology, 48, 525–545.
• Greenberg J. T, Yao, N. (2004). The role and regulation of programmed cell death in plant–pathogen interactions. Cellular Microbiology, 6, 201–211.
• Halliwell B and Gutteridge J M C (2002). Free radicals in biology and medicine 3rd edition (Oxford, UK: Oxford University Press)
• Hammond-Kosack KE , Parker JE (2003). Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding . Curr Opin Biotechnol 14 : 177 – 193
• Heitefuss R. (1997). Cell wall modification in relation to resistance. In H. Hartleb, R. Heitefuss, H.-H. Hoppe (Eds.), Resistance of crop plants against fungi (pp. 100– 125). Jena: Gustav Fischer.
• HpaG identifies a key functional region that elicits the hypersensitive response in nonhost plants. J. Bacteriol. 2004, 186, 6239–6247.
• Huckelhoven R, Kogel K-H (2003). Reactive oxygen intermediates in plantmicrobe interactions: Who is who in powdery mildew resistance? Planta 216: 891–902.
• Ishiga Y, Uppalapati SR, Ishiga T, Elavarthi S, Martin B & Bender CL (2008). The phytotoxin coronatine induces lightdependent reactive oxygen species in tomato seedlings. New Phytol 181: 147–160.
• Ishiga Y, Uppalapati SR, Ishiga T, Elavarthi S, Martin B & Bender CL (2009). Involvement of coronatine-inducible reactive oxygen species in bacterial speck disease of tomato. Plant Signal Behav 4: 237–239.
• Jabs T, Tschöpe, M., Colling C., Hahlbrock K., Scheel D (1997). Elicitor-stimulated ion fluxes and O_ 2 from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proceedings of the National Academy of Sciences of the United States of America, 94, 4800–4805.
• Jones A(2000). Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends Plant Sci. 5 225–230.
• Jones J.D, Dangl, J.L. (2006). The plant immune system. Nature, 444, 323–329.
• Joo, J. H., Y. S. Bae, and, (2001). J. S. Lee, “Role of auxin-induced reactive oxygen species in root gravitropism,” Plant Physiology, vol. 126, no. 3, pp. 1055-1060
• Jorgensen H. J. L., Lübeck, P. S., Thordal-Christensen, H., de Neergaard, E., & Smedegaard-Petersen, V. (1998). Mechanisms of induced resistance in barley against Drechslera teres. Phytopathology, 88, 698–707.
• Kanzaki H , Saitoh H , Ito A , Fujisawa S , Kamoun S , Katou S , Yoshioka H , Terauchi R (2003). Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana . Mol Plant Pathol 4: 383 – 391
• Kariola T, Palomäki T.A, Brader G, Palva E.T (2003). Erwinia carotovora subsp. carotovora and Erwinia -derived elicitors HrpN and PehA trigger distinct but interacting defense responses and cell death in Arabidopsis. Mol. Plant-Microbe Interact.16, 179–187.
• Keith LMW, Bender CL (1999). AlgT (r22) controls alginate production and tolerance to environmental stress in Pseudomonas syringae. J Bacteriol 181: 7176–7184.
• Keith RC, Keith LMW, Herna´ndez-Guzma´n G, Uppalapati SR & Bender CL (2003). Alginate gene expression by Pseudomonas syringae pv. tomato DC3000 in host and nonhost plants. Microbiology 149: 1127–1138.
• Kieffer F, Jherminier J, Simon-Plas F, Nicole M, Paynot M, Elmayan T and Blein J ( 2000). The fungal elicitor cryptogein induces cell wall modifi cations on tobacco cell suspension; J. Exp. Bot. 51 1799–1811
• Kim YC, Miller CD & Anderson AJ (1999). Transcriptional regulation by iron and role during pathogenesis of genes encoding iron and manganese superoxide dismutases of Pseudomonas syringae pv. syringae. Physiol Mol Plant Pathol 55: 327–339.
• Kim, J.G.; Jeon, E.; Oh, J.; Moon, J.S.; Hwang, I. Mutational analysis of Xanthomonas harpin
• Kohanski MA, Dwyer DJ, Hayete B, Lawrence, CA, Collins JJ (2007). A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130: 797–810.
• Lam E (2004). Controlled cell death, plant survival and development. Nature Reviews in Molecular Cell Biology, 5, 305–315.
• Lamb C, Dixon RA (1997). The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251–275
• Lawton, M.; Saidasan, H. Pathogenesis in mosses. Annu. Plant Rev. (2009). 36, 298–339.
• Legendre L, Rueter, S., Heinstein, P S, Low, P S (1993). Characterisation of the oligogalacturonide-induced oxidative burst in cultured soybean (Glycine max) cells. Plant Physiology, 102, 233–240.
• Li J, Zhang, Z.-G., Ji, R., Wang, Y.-C, Zheng, X.-B (2006). Hydrogen peroxide regulates elicitor PB90-induced cell death and defense in non-heading Chinese cabbage. Physiological and Molecular Plant Pathology, 67, 220–230.
• Link T, Lohaus, G., Heiser, I., Mendgen, K., Hahn, M., & Voegele, R. T. (2005). Characterization of a novel NADP+-dependent D-arabitol dehydrogenase from the plant pathogen Uromyces fabae. Biochemical Journal, 389, 289–295.
• Love AJ, Yun B-W, Laval V, Loake GJ, Milner JL (2005). Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol 139: 935–948
• Mach JM, Castillo AR, Hoogstraten R, Greenberg JT. (2001) . The Arabidopsis accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc. Natl. Acad. Sci. USA 98: 771–76.
• Maheshwari, R. and R. S. Dubey ( 2009). “Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings,” Plant Growth Regulation, vol. 59, no. 1, pp. 37-49
• Mayer, A. M., Staples, R. C., & Gil-ad, N. L. (2001). Mechanisms of survival of necrotrophic fungal plant pathogens in hosts expressing the hypersensitive response. Phytochemistry, 58, 33–41.
• Mazau D and Esquerré-Tugayé M T (1986). Hydroxyproline-rich glycoprotein accumulation in the cell walls of plants infected by various pathogens; Physiol. Mol. Plant Pathol. 29 147–157
• Mellersh, D. G., Foulds, I. V., Higgens, V. J., & Heath, M. C. (2002). H2O2 plays different roles in determining penetration failure in three diverse plant–fungal interactions. The Plant Journal, 29, 257–268.
• Meyers BC, Kaushik S, Nandety RS (2005). Evolving disease resistance genes . Curr Opin Plant Biol 8: 129 – 134
• Miller G, Shulaev V, and Mittler R (2008). “Reactive oxygen signaling and abiotic stress,” Physiologia Plantarum, vol. 133, no. 3, pp. 481-489
• Mishra, S., A. B. Jha, and R. S. Dubey,( 2011). “Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings,” Protoplasma, vol. 248, no. 3, pp. 565-577
• Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004). Reactive oxygen gene network of plants. Trends Plant Sci 9: 490–498 Moeder W, Yoshioka K, Klessig DF (2005) Involvement of the small GTPase Rac in the defense responses of tobacco to pathogens. Mol Plant Microbe Interact 18: 116–124
• Mittler R (2002). “Oxidative stress, antioxidants and stress tolerance,” Trends in Plant Science, vol. 7, no.9, pp. 405-410
• Mittler R., E. H. Herr, B. L. Orvar, et al. (1999). “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
• Mittler R, Vanderauwera, S., Gollery, M., Van Breusegem, F (2004). The reactive oxygen gene network in plants. Trends in Plant Science, 9, 490–498.
• Montillet J-L, Chamnongpol S, Rusterucci C, Dat J, van de Cotte B, Agnel J-P, Battesti C, Inze D, Van Breusegem F, Triantaphylides C (2005). Fatty acid hydroperoxides and H2O2 in the execution of hypersensitive cell death in tobacco leaves. Plant Physiol 138: 1516–1526
• Moon H, Lee B, Choi G, Shin D, Prasad D T, Lee O, Kwak S -S, Kim D H, Nam J, Bahk J, Hong J C, Lee S Y, Cho M Je and Lim C Oh (2003). NDP kinase 2 interacts with two oxidative stressactivated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants; Proc. Natl. Acad. Sci. USA 100 358–363
• Morel J, Fromentin J, Blein JP, Simon-Plas F, Elmayan T (2004). Rac regulation of NtrbohD, the oxidase responsible for the oxidative burst in elicited tobacco cell. Plant J 37: 282–293
• Mou Z, Fan W, Dong X. (2003). Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–44
• Nanda K, A. Emilie, M. Daniel, N. Pauly, and C. Dunand ( 2010). “Reactive oxygen species during plant-microorganism early interactions,” Journal of Integrative Plant Biology, vol. 52, no. 2, pp. 195-204
• Nandini P. Shetty Hans J. Lyngs Jorgensen, Jens Due Jensen, David B. Collinge, H. Shekar Shetty(2008). Roles of reactive oxygen species in interactions between plants and pathogens Eur J Plant Pathol 121:267–280
• Noctor G. and C. Foyer (1998). “Ascorbate and glutathione: Keeping active oxygen under control,” Annual Review of Plant Physiology and Plant Molecular Biology, vol. 49, pp. 249-279
• Noctor G., S. Veljovic-Jovanovic, S. Driscoll, L. Novitskaya, and C. H. Foyer ( 2002). “Drought and oxidative load in the leaves of C3 plants: A predominant role for photorespiration?” Annals of Botany, vol. 89, no. 7, pp. 841-850
• Nurnberger T, Brunner F, Kemmerling B, Piater L (2004). Innate immunity in plants and animals: Striking similarities and obvious differences. Immunological Rev 198: 249 – 266
• Nurnberger, T. M., Nennsteil, O., Jabs, T., Sacks, W. R., Hahlbrock, K., & Scheel, D. (1994). High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell, 78, 449–460.
• Oliver, R. P., & Ipcho, S. V. S. (2004). Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Molecular Plant Pathology, 4, 347–352.
• Ono E, Wong HL, Kawasaki T, Hasegawa M, Kodama O, Shimamoto K (2001). Essential role of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci USA 98: 759–764
• Pang C. H, Wang B S (2008). “Oxidative stress and salt tolerance in plants,” in Progress in Botany, U. Lüttge, W. Beyschlag, and J. Murata, Eds., pp. 231-245, Springer-Verlag, Berlin, Heidelberg
• Pavet V, Olmos E, Kiddle G, Mowla S, Kumar S, Antoniw J, Alvarez M E and Foyer C H (2005). Ascorbic acid defi ciency activates cell death and disease resistance responses in Arabidopsis; Plant Physiol. 139 1291–1303
• Perumalla C J, Heath M C (1991). The effect of inhibitors of various cellular processes on the wall modifi cations induced in bean leaves by the cowpea rust fungus; Physiol. Mol. Plant Pathol. 38 293–300
• Petit J-M, Briat J-F, Lobr´eaux S. (2001) .Structure and differential expression of the four members of the Arabidopsis thaliana ferritin gene family. Biochem. J. 359:575–82
• Pnueli L, Hongjian L and Mittler R (2003). Growth suppression, abnormal guard cell response, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants; Plant J. 34 187–203
• Polidoros AN, Mylona PV, Scandalios JP (2001). Transgenic tobacco plants expressing the maize Cat2 gene have altered catalase levels that affect plant-pathogen interactions and resistance to oxidative stress. Transgenic Res 10: 555–569
• Polidoros AN, MylonaPV, Scandalios JG. (2001). Transgenic tobacco plants expressing the maize Cat2 gene have altered catalase levels that affect plant-pathogen interactions and resistance to oxidative stress. Transgenic Res. 10:555–69
• Radwan D. E. M., K. A. Fayez, S. Y. Mahmoud, and G. Lu ( 2010). “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
• Ramanjulu S, Bartels D (2002). Drought- and desiccation-inducedmodulation of gene expression in plants; Plant Cell Environ. 25 141–151
• Rao M V and Davis R D (1999). Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid; Plant J. 17 603–614
• Rizhsky L, Davletova S, Liang H and Mittler R (2004). The zinc fi nger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis; J. Biol. Chem. 279 11736–11743
• Santos R, Franza T, Laporte ML, Sauvage C, Touati D & Expert D (2001). Essential role of superoxide dismutase on the pathogenicity of Erwinia chrysanthemi strain 3937. Mol Plant Microbe Interact 14: 758–767.
• Sasaki K, Iwai T, Hiraga S, Kuroda K, Seo S, Mitsuhara I, Miyasaka A, IwanoM, Ito H, Matsui H, et al (2004). Ten rice peroxidases redundantly respond to multiple stresses including infection with rice blast fungus. Plant Cell Physiol 45: 1442–1452
• Sasaki K., T. Iwai, Hiraga S ( 2004). “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
• Sasaki, K., T. Iwai, S. Hiraga, et al. (2004). “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
• Scheideler M, Schlaich N L, Fellenberg K, Beissbarth T, Hauser N C, Vingron M, Slusarenko A J and Hoheisel J D (2002). Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays; J. Biol. Chem. 277 10555–10561
• Schultheiss H, Dechert C, Kogel K-H, Huckelhoven R (2003). Functional analysis of barley RAC/ROP G-protein family members in susceptibility to the powdery mildew fungus. Plant J 36: 589–601
• Schulze-Lefert P (2004). Knocking on the heaven's wall: Pathogenesis of and resistance to biotrophic fungi at the cell wall. Current Opinion in Plant Biology, 7, 377–383.
• Schweizer P, Christoffel A and Dudler R (1999). Transient expression of members of the germin-like gene family in epidermal cells of wheat confers disease resistance; Plant J. 20 541–552
• Semchuk N. M., O. V. Lushchak, J. Falk, K. Krupinska, and V. I. Lushchak ( 2009). “ 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
• Shah K., R. G. Kumar, S. Verma, and R. S. Dubey “Effect of ( 2001). 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
• Sharma P., A. B. Jha, and R. S. Dubey (2010). “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, Florida, USA, 3rd edition
• Shetty N. P. Kristensen, B. K., Newman, M.-A., Møller, K., Gregersen, P. L., Jorgensen, H. J. L. (2003). Association of hydrogen peroxide with restriction of Septoria tritici in resistant wheat. Physiological and Molecular Plant Pathology, 62, 333–346.
• Shetty N. P. Mehrabi, R., Lütken, H., Haldrup, A., Kema, G. H. J., Collinge, D. B., (2007). Role of hydrogen peroxide during the interaction between the hemibiotrophic fungal pathogen Septoria tritici and wheat. New Phytologist, 174, 637–647.
• Simeon O Kotchoni and Emma W Gachomo(2006). The reactive oxygen species network pathways: an essential prerequisite for perception of pathogen attack and the acquired disease resistance in plants J. Biosci. 31(3)
• Soto MJ, Sanjua´n J, Olivares J (2006). Rhizobia and plantpathogenic bacteria: common infection weapons. Microbiology 152: 3167–3174.
• Soylu S, Brown I, Mansfield JW (2005). Cellular reactions in Arabidopsis following challenge by strains of Pseudomonas syringae: from basal resistance to compatibility. Physiol Molec Plant Pathol 66: 232–243
• Spoel S H Koornnef A, Claessens S M C, Korzelius J P et al (2003). NPR1 modulates cross-talk between salicylate- and jasmonatedependent defense pathways through a novel function in the cytosol; Plant Cell 15 760–770
• Thordal-Christensen, H., Zhang, Z., Wei, Y., & Collinge, D. B. (1997). Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley–powdery mildew interaction. The Plant Journal, 11, 1187–1194.
• Torres MA, Dangl JL (2005). Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8: 397–403
• Torres MA, Dangl JL, Jones JD (2002). Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99: 517–522
• Torres M. A., J. L. Dangl, and J. D. G. Jones (2002). “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
• Torres M. A., Jones, J D G., Dangl, J L (2006). Reactive oxygen species signaling in response to pathogens. Plant Physiology, 141, 373–378.
• Trujillo M, Altschmeid, L., Schweizer, P, Kogel, K.-H, Hückelhoven R (2006). Respiratory Burst Oxidase Homologue A of barley contributes to penetration by the powdery mildew fungus Blumeria graminis f. sp. hordei. Journal of Experimental Botany, 57, 3781–3791.
• Tyres M and Mann M (2003). From genomics to proteomics; Nature(London) 422 193–197
• Uppalapati SR, Ishiga Y, Wangdi T, Urbanczyk-Wochniak E, Ishiga T, Mysore KS, Bender CL (2008) Pathogenicity of Pseudomonas syringae pv. tomato on tomato seedlings: phenotypic and gene expression analyses of the virulence function of coronatine. Mol PlantMicrobe Interact 21: 383–395.
• Van Breusegem F, Dat, J F (2006). Reactive oxygen species in plant cell death. Plant Physiology, 141, 384–390.
• van Doorn W.G, Beers, E.P.; Dangl J.L, Franklin-Tong, V.E.; Gallois, P, Hara-Nishimura, I, Jones A.M, Kawai-Yamada M, Lam E, Mundy J (2011). Morphological classification of plant cell deaths. Cell Death Differ. 18, 1241–1246.
• van Loon LC, Rep M, Pieterse CMJ (2006). Significance of inducible defense-related proteins in infected plants . Annu Rev Phytopathol 44 : 135 – 162
• Vanacker H, Carver TLW, Foyer CH (1998). Pathogen induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol 117: 1103–1114.
• Veronese P, Nakagami H, Bluhm B, AbuQamar S, Chen X, Salmeron J, Dietrich R A, Hirt H and Mengiste T (2006). The membrane-anchored Botrytis-induced kinase1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens; Plant Cell 18 257–273
• Wojtaszek P (1997). “Oxidative burst: an early plant response to pathogen,” Biochemical Journal, vol. 322, no. 3, pp. 681-692
• Wu, G. S., Short, B. J., Lawrence, E. B., Levine, E. B., Fitzsimmons, K. C., & Shah, D. M. (1995). Disease resistance conferred by expression of a gene encoding H2O2-generating glucose oxidase in transgenic potato plants. The Plant Cell, 7, 1357–1368.
• Zhao Y, Thilmony R, Bender CL, Schaller A, He SY, Howe GA (2003). Virulence systems in Pseudomonas syringae pv. tomato promote bacterial speck disease by targeting the jasmonate signalling pathway. Plant J 36: 485–499.