Skip to main content

Signaling role of reactive oxygen species in plants under stress

Abstract

The review considers the role of H2O2, 1O2, O ·−2 , and the products of lipid peroxidation as signaling molecules in the processes of stress signal transduction in plants. The data concerning possible ROS participation in transduction of stress signals from chloroplasts to the nuclear genome, H2O2 involvement in transduction stress signals in cyanobacteria, and also the interactions between ROS and other signaling systems within the cell are presented. It is suggested that redox regulators, protein kinases/protein phosphatases, and transcription factors play a crucial role in the functioning of ROS-dependent signaling systems in the plant cell.

This is a preview of subscription content, access via your institution.

Abbreviations

IP3 :

inositol 1,4,5-triphosphate

MAPK:

mitogen-activated protein kinase

OS:

oxidative stress

POL:

peroxidation of lipids

PQ:

plastoquinone pool

PS:

photosystem

PUFA:

polyunsaturated fatty acids

RC:

reaction center

SOD:

superoxide dismutase

References

  1. 1.

    Kolupaev, Yu.E. and Karpets, Yu.V., Formirovanie adaptivnykh reaktsii rastenii na deistvie abioticheskikh stressov (Formation of Adaptive Plant Responses to Abiotic Stresses), Kiev: Osnova, 2010.

    Google Scholar 

  2. 2.

    Apel, K. and Hirt, H., Reactive Oxygen Species: Metabolism, Oxidative Stress, and Signal Transduction, Annu. Rev. Plant Biol., 2004, vol. 55, pp. 373–399.

    PubMed  Article  CAS  Google Scholar 

  3. 3.

    Asada, K., The Water-Water Cycle in Chloroplasts: Scavenging of Active Oxygens and Dissipation of Excess Photons, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1999, vol. 50, pp. 601–639.

    PubMed  Article  CAS  Google Scholar 

  4. 4.

    Chen, Z., Silva, H., and Klessig, D.F., Active Oxygen Species in the Induction of Plant Systemic Acquired Resistance by Salicylic Acid, Science, 1993, vol. 262, pp. 1883–1886.

    PubMed  Article  CAS  Google Scholar 

  5. 5.

    Minibayeva, F., Kolesnikov, O.P., and Gordon, L.K., Contribution of a Plasma Membrane Redox System to the Superoxide Production by Wheat Root Cells, Protoplasma, 1998, vol. 205, pp. 101–106.

    Article  CAS  Google Scholar 

  6. 6.

    Minibaeva, F.V. and Gordon, L.Kh., Superoxide Production and the Activity of Extracellular Peroxidase in Plant Tissues under Stress Conditions, Russ. J. Plant Physiol., 2003, vol. 50, pp. 411–416.

    Article  CAS  Google Scholar 

  7. 7.

    Desikan, R., Mackerness, S.A.-H., Hancock, J.T., and Neill, S.J., Regulation of the Arabidopsis Transcriptome by Oxidative Stress, Plant Physiol., 2001, vol. 127, pp. 159–172.

    PubMed  Article  CAS  Google Scholar 

  8. 8.

    Desikan, R., Hancock, J.T., and Neill, S.J., Oxidative Stress Signaling, Plant Responses to Abiotic Stress: Topic in Current Genetics, Hirt, H. and Shinozaki, K., Eds., New York: Springer-Verlag, 2003, pp. 121–148.

    Chapter  Google Scholar 

  9. 9.

    Mori, I.C. and Schroeder, J.I., Reactive Oxygen Species Activation of Plant Ca2+ Channels: A Signaling Mechanism in Polar Growth, Hormone Transduction, Stress Signaling, and Hypothetically Mechanotransduction, Plant Physiol., 2004, vol. 135, pp. 702–708.

    PubMed  Article  CAS  Google Scholar 

  10. 10.

    Foyer, C.H. and Noctor, G., Redox Homeostis and Antioxidant Signaling: A Metabolic Interface between Stress Perception and Physiological Responses, Plant Cell, 2005, vol. 17, pp. 1866–1875.

    PubMed  Article  CAS  Google Scholar 

  11. 11.

    Galvez-Valdivieso, G. and Mullineaux, P.M., The Role of Reactive Oxygen Species in Signalling from Chloroplasts to the Nucleus, Physiol. Plant., 2010, vol. 138, pp. 430–439.

    PubMed  Article  CAS  Google Scholar 

  12. 12.

    Pei, Z.-M., Murata, Y., Benning, G., Thomine, S., Klusener, B., Allen, G.J., Grill, E., and Schroeder, J.I., Calcium Channels Activated by Hydrogen Peroxide Mediate Abscisic Acid Signalling in Guard Cells, Nature, 2000, vol. 406, pp. 731–734.

    PubMed  Article  CAS  Google Scholar 

  13. 13.

    Jaspers, P. and Kangasjarvi, J., Reactive Oxygen Species in Abiotic Stress Signaling, Physiol. Plant., 2010, vol. 138, pp. 405–413.

    PubMed  Article  CAS  Google Scholar 

  14. 14.

    Shao, N., Beck, C.F., Lemaire, S.D., and Krieger-Liszkay, A., Photosynthetic Electron Flow Affects H2O2 Signaling by Inactivation of Catalase in Chlamydomonas reinhardtii, Planta, 2008, vol. 228, pp. 1055–1066.

    PubMed  Article  CAS  Google Scholar 

  15. 15.

    Pfannschmidt, T., Bräutigam, K., Wagner, R., Dietzel, L., Schröter, Y., Steiner, S., and Nykytenko, A., Potential Regulation of Gene Expression in Photosynthetic Cells by Redox and Energy State: Approaches towards Better Understanding, Ann. Bot., 2009, vol. 103, pp. 599–607.

    PubMed  Article  CAS  Google Scholar 

  16. 16.

    Mullineaux, P.M., Karpinski, S., and Baker, N.R., Spatial Dependence for Hydrogen Peroxide-Directed Signaling in Light-Stressed Plants, Plant Physiol., 2006, vol. 141, pp. 346–350.

    PubMed  Article  CAS  Google Scholar 

  17. 17.

    Pitzschke, P. and Hirt, H., Mitogen-Activated Protein Kinases and Reactive Oxygen Species Signaling in Plants, Plant Physiol., 2006, vol. 141, pp. 351–356.

    PubMed  Article  CAS  Google Scholar 

  18. 18.

    Miller, G., Nobuhiro, S., Rizhsky, L., Hegie, A., Koussevitzky, S., and Mittler, R., Double Mutants Deficient in Cytosolic and Thylakoid Ascorbate Peroxidase Reveal a Complex Mode of Interaction between Reactive Oxygen Species, Plant Development, and Response to Abiotic Stresses, Plant Physiol., 2007, vol. 144, pp. 1777–1785.

    PubMed  Article  CAS  Google Scholar 

  19. 19.

    Swanson, S. and Gilroy, S., ROS in Plant Development, Physiol. Plant., 2010, vol. 138, pp. 384–392.

    PubMed  Article  CAS  Google Scholar 

  20. 20.

    Foyer, C.H. and Shigeoka, S., Understanding Oxidative Stress and Antioxidant Functions to Enhance Photosynthesis, Plant Physiol., 2011, vol. 155, pp. 93–100.

    PubMed  Article  CAS  Google Scholar 

  21. 21.

    Foyer, C.H. and Noctor, G.D., Redox Regulation in Photosynthetic Organisms: Signalling, Acclimation, and Practical Implications, Antiox. Redox Signal., 2009, vol. 11, pp. 861–905.

    Article  CAS  Google Scholar 

  22. 22.

    Khavinson, V.K., Barinov, V.A., Arutyunyan, A.V., and Malinin, V.V., Svobodnoradikal’noe okislenie i starenie (Free Radial Oxidation and Aging), St. Petersburg: Nauka, 2003.

    Google Scholar 

  23. 23.

    Ivanov, B.N., Mubarakshina, M.M., and Khorobrykh, S.A., Kinetics of the Plastoquinone Pool Oxidation Following Illumination. Oxygen Incorporation into Photo-synthetic Electron Transport Chain, FEBS Lett., 2007, vol. 581, pp. 1342–1346.

    PubMed  Article  CAS  Google Scholar 

  24. 24.

    Pospisil, P., Production of Reactive Oxygen Species by Photosystem II, Biochim Biophys. Acta, 2009, vol. 1787, pp. 1151–1160.

    PubMed  Article  CAS  Google Scholar 

  25. 25.

    Krieger-Liszkay, A., Singlet Oxygen Production in Photosynthesis, J. Exp. Bot., 2005, vol. 56, pp. 337–346.

    PubMed  Article  CAS  Google Scholar 

  26. 26.

    Mittler, R., Oxidative Stress, Antioxidants and Stress Tolerance, Trends Plant Sci., 2002, vol. 7, pp. 405–410.

    PubMed  Article  CAS  Google Scholar 

  27. 27.

    Karu, T.I., Mitochondrial Signaling in Mammalian Cells Activated by Red and Near-IR Radiation, Photochem. Photobiol., 2008, vol. 84, pp. 1091–1099.

    PubMed  Article  CAS  Google Scholar 

  28. 28.

    Allakhverdiev, S.I., Los, D.A., Mohanty, P., Nishiyama, Y., and Murata, N., Glycinebetaine Alleviates the Inhibitory Effect of Moderate Heat Stress on the Repair of Photosystem II during Photoinhibition, Biochim. Biophys. Acta, 2007, vol. 1767, pp. 1363–1371.

    PubMed  Article  CAS  Google Scholar 

  29. 29.

    Kreslavski, V.D., Carpentier, R., Klimov, V.V., and Allakhverdiev, S.I., Transduction Mechanisms of Photoreceptor Signals in Plant Cells, J. Photochem. Photobiol. C. Photochem. Rev., 2009, vol. 10, pp. 63–80.

    Article  CAS  Google Scholar 

  30. 30.

    Hung, S.-H., Yu, C.-W., and Lin, C.H., Hydrogen Peroxide Functions as a Stress Signal in Plants, Bot. Bull. Acad. Sinica, 2005, vol. 46, pp. 1–10.

    CAS  Google Scholar 

  31. 31.

    Pradedova, E.V., Isheeva, O.D., and Salyaev, R.K., Classification of the Antioxidant Defense System as the Ground for Reasonable Organization of Experimental Studies of the Oxidative Stress in Plants, Russ. J. Plant Physiol., 2011, vol. 58, pp. 210–217.

    Article  CAS  Google Scholar 

  32. 32.

    Ishikawa, T. and Shigeoka, S., Recent Advances in Ascorbate Biosynthesis and the Physiological Significance of Ascorbate Peroxidase in Photosynthesizing Organisms, BoiSci. Biotechnol. Biochem., 2008, vol. 72, pp. 1143–1154.

    Article  CAS  Google Scholar 

  33. 33.

    Sairam, R.K. and Srivastava, G.C., Induction of Oxidative Stress and Antioxidant Activity by Hydrogen Peroxide Treatment in Tolerant and Susceptible Wheat Genotypes, Biol. Plant., 2000, vol. 43, pp. 381–386.

    Article  CAS  Google Scholar 

  34. 34.

    Kreslavskii, V.D., Carpentier, R., Klimov, V.V., Murata, N., and Allakhverdiev, S.I., Molecular Mechanisms for Photosynthetic Apparatus Resistance to Stress, Biol. Membr. (Moscow), 2007, vol. 24, pp. 195–217.

    Google Scholar 

  35. 35.

    Kuznetsov, Vl.V. and Shevyakova, N.I., Proline under Stress: Biological Role, Metabolism, and Regulation, Russ. J. Plant Physiol., 1999, vol. 46, pp. 274–288.

    CAS  Google Scholar 

  36. 36.

    Tarchevsky, I.A., Metabolizm rastenii pri stresse (Plant Metabolism under Stress), Kazan: Fen, 2001.

    Google Scholar 

  37. 37.

    Kuznetsov, Vl.V. and Shevyakova, N.I., Polyamines and Stress Tolerance of Plants, Plant Stress, 2007, vol. 1, pp. 50–71.

    Google Scholar 

  38. 38.

    Vranova, E., Inze, D., and van Breusegem, F., Signal Transduction during Oxidative Stress, J. Exp. Bot., 2002, vol. 53, pp. 1227–1236.

    PubMed  Article  CAS  Google Scholar 

  39. 39.

    Kreslavskii, V.D., Lyubimov, V.Yu., Kotova, L.M., and Kotov, A.A., Effect of Common Bean Seedling Pretreatment with Chlorocholine Chloride on Photosystem II Tolerance to UV-B Radiation, Phytohormone Content, and Hydrogen Peroxide Content, Russ. J. Plant Physiol., 2011, vol. 58, pp. 324–329.

    Article  CAS  Google Scholar 

  40. 40.

    Spadaro, D., Yun, B.-W., Spoel, S.H., Chu, C., Wang, Y.-Q., and Loake, G.J., The Redox Switch: Dynamic Regulation of Protein Function by Cysteine Modifications, Physiol. Plant., 2010, vol. 138, pp. 360–371.

    PubMed  Article  CAS  Google Scholar 

  41. 41.

    Kojima, K., Oshita, M., Nanjo, Y., Kasai, K., Tozawa, Y., Hayashi, H., and Nishiyama, Y., Oxidation of Elongation Factor G Inhibits the Synthesis of the D1 Protein of Photosystem II, Mol. Microbiol., 2007, vol. 65, pp. 936–947.

    PubMed  Article  CAS  Google Scholar 

  42. 42.

    Kojima, K., Motohashi, K., Morota, T., Oshita, M., Hisabori, T., Hayashi, H., and Nishiyama, Y., Regulation of Translation by the Redox State of Elongation Factor G in the Cyanobacterium Synechocystis sp. PCC 6803, J. Biol. Chem., 2009, vol. 284, pp. 18 685–18 691.

    Article  CAS  Google Scholar 

  43. 43.

    Nishiyama, Y., Allakhverdiev, S.I., and Murata, N., Protein Synthesis Is the Primary Target of Reactive Oxygen Species in the Photoinhibition of Photosystem II, Physiol. Plant., 2011, vol. 142, pp. 35–46.

    PubMed  Article  CAS  Google Scholar 

  44. 44.

    Zhang, L., Paakkarinen, V., van Wijk, K.J., and Aro, E.-M., Biogenesis of the Chloroplast-Encoded D1 Protein: Regulation of Translation Elongation, Insertion and Assembly into Photosystem II, Plant Cell, 2000, vol. 12, pp. 1769–1782.

    PubMed  Article  CAS  Google Scholar 

  45. 45.

    Mittler, R., Vanderauwera, S., Gollery, M., and van Breusegem, F., Reactive Oxygen Gene Network of Plants, Trends Plant Sci., 2004, vol. 9, pp. 490–498.

    PubMed  Article  CAS  Google Scholar 

  46. 46.

    Davletova, S., Rizhsky, L., Liang, H., Shengqiang, Z., Oliver, D.J., Coutu, J., Shulaev, V., Schlauch, K., and Mittler, R., Cytosolic Ascorbate Peroxidase 1 Is a Central Component of the Reactive Oxygen Gene Network of Arabidopsis, Plant Cell, 2005, vol. 17, pp. 268–281.

    PubMed  Article  CAS  Google Scholar 

  47. 47.

    Buchanan, B.B. and Luan, S., Redox Regulation in the Chloroplast Thylakoid Lumen: A New Frontier in Photosynthesis Research, J. Exp. Bot., 2005, vol. 56, pp. 1439–1447.

    PubMed  Article  CAS  Google Scholar 

  48. 48.

    Shao, N., Krieger-Liszkay, A., Schroda, M., and Beck, C.F., A Reporter System for the Individual Detection of Hydrogen Peroxide and Singlet Oxygen: Its Use for the Assay of Reactive Oxygen Species Produced In Vivo, Plant J., 2007, vol. 50, pp. 475–487.

    PubMed  Article  CAS  Google Scholar 

  49. 49.

    Fey, V., Wagner, R., Brütigam, K., and Pfannschmidt, T., Photosynthetic Redox Control of Nuclear Gene Expression, J. Exp. Bot., 2005, vol. 56, pp. 1491–1498.

    PubMed  Article  CAS  Google Scholar 

  50. 50.

    Pogson, B.J., Woo, N.S., Förster, B., and Small, I.D., Plastid Signalling to the Nucleus and beyond, Trends Plant Sci., 2008, vol. 13, pp. 602–609.

    PubMed  Article  CAS  Google Scholar 

  51. 51.

    Yang, D.-H., Andersson, B., Aro, E.M., and Ohad, I., The Redox State of the Plastoquinone Pool Controls the Level of the Light-Harvesting Chlorophyll a/b Binding Protein Complex II (LHC II) during Photoacclimation, Photosynth. Res., 2001, vol. 68, pp. 163–174.

    PubMed  Article  CAS  Google Scholar 

  52. 52.

    Scheibe, R., Backhausen, J.E., Emmerlich, V., and Holtgrefe, S., Strategies to Maintain Redox Homeostasis during Photosynthesis under Changing Conditions, J. Exp. Bot., 2005, vol. 56, pp. 1481–1489.

    PubMed  Article  CAS  Google Scholar 

  53. 53.

    Lee, K.P., Kim, C., Langraf, F., and Apel, K., EXECUTER1- and EXECUTER2-Dependent Transfer of Stress-Related Signals from the Plastid to the Nucleus of Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA, 2007, vol. 104, pp. 10 270–10 275.

    CAS  Google Scholar 

  54. 54.

    Danon, A., Miersch, O., Felix, G., Camp, R.G., and Apel, K., Concurrent Activation of Cell Death-Regulating Signaling Pathways by Singlet Oxygen in Arabidopsis thaliana, Plant J., 2005, vol. 41, pp. 68–80.

    PubMed  Article  CAS  Google Scholar 

  55. 55.

    Bienert, G.P., Müller, A.L., Kristiansen, K.A., Schulz, A., Müller, I.M., Schjoerring, J.K., and Jahn, T.P., Specific Aquaporins Facilitate the Diffusion of Hydrogen Peroxide across Membranes, J. Biol. Chem., 2007, vol. 282, pp. 1183–1192.

    PubMed  Article  CAS  Google Scholar 

  56. 56.

    Davletova, S., Schlauch, K., Coutu, J., and Mittler, R., The Zinc-Finger Protein ZAT12 Plays a Central Role in Reactive Oxygen and Abiotic Stress Signaling in Arabidopsis, Plant Physiol., 2005, vol. 139, pp. 847–856.

    PubMed  Article  CAS  Google Scholar 

  57. 57.

    Karpinski, S., Reynolds, H., Karpinska, B., Wingsle, G., Creissen, G., and Mullineaux, P., Systemic Signalling and Acclimation in Response to Excess Excitation Energy in Arabidopsis, Science, 1999, vol. 284, pp. 654–657.

    PubMed  Article  CAS  Google Scholar 

  58. 58.

    Mubarakshina, M.M., Ivanov, B.N., Naidov, I.A., Hillier, W., Badger, M.R., and Krieger-Liszkay, A., Production and Diffusion of Chloroplastic H2O2 and Its Implication to Signalling, J. Exp. Bot., 2010, vol. 61, pp. 3577–3587.

    PubMed  Article  CAS  Google Scholar 

  59. 59.

    Bechtold, U., Richard, O., Zamboni, A., Gapper, C., Geisler, M., Pogson, B., Karpinski, S., and Mullineaux, P.M., Impact of Chloroplastic- and Extracellular-Sourced ROS on High Light-Responsive Gene Expression in Arabidopsis, J. Exp. Bot., 2008, vol. 59, pp. 121–133.

    PubMed  Article  CAS  Google Scholar 

  60. 60.

    Mullineaux, P., Ball, L., Escobar, C., Karpinska, B., Creissen, G., and Karpinski, S., Are Diverse Signalling Pathways Integrated in the Regulation of Arabidopsis Antioxidant Defense Gene Expression in Response to Excess Excitation Energy? Phil. Transact. R. Soc. London, 2000, vol. 355, pp. 1531–1540.

    Article  CAS  Google Scholar 

  61. 61.

    Kaluev, A.V., On the Problem of a Regulatory Role of Active Oxygen Species in Cells, Biochemistry (Moscow), 1998, vol. 63, pp. 1114–1115.

    CAS  Google Scholar 

  62. 62.

    Yabuta, Y., Maruta, T., Yoshimura, K., Ishikawa, T., and Shigeoka, S., Two Distinct Redox Signaling Pathways for Cytosolic APX Induction under Photooxidative Stress, Plant Cell Physiol., 2004, vol. 45, pp. 1586–1594.

    PubMed  Article  CAS  Google Scholar 

  63. 63.

    Laloi, C., Stachowiak, M., Pers-Kamczyc, E., Warzych, E., Murgia, I., and Apel, K., Cross-Talk between Singlet Oxygen- and Hydrogen Peroxide-Dependent Signaling of Stress Responses in Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA, 2007, vol. 104, pp. 672–677.

    PubMed  Article  CAS  Google Scholar 

  64. 64.

    Karpinska, B., Wingsle, G., and Karpinski, S., Antagonistic Effects of Hydrogen Peroxide and Glutathione on Acclimation to Excess Excitation Energy in Arabidopsis, IUBMB Life, 2000, vol. 50, pp. 21–26.

    PubMed  Article  CAS  Google Scholar 

  65. 65.

    Kanesaki, Y., Yamamoto, H., Paithoonrangsarid, K., Shoumskaya, M., Suzuki, I., Hayashi, H., and Murata, N., Histidine Kinases Play Important Roles in the Perception and Signal Transduction of Hydrogen Peroxide in the Cyanobacterium, Synechocystis sp. PCC 6803, Plant J., 2007, vol. 49, pp. 313–324.

    PubMed  Article  CAS  Google Scholar 

  66. 66.

    Suzuki, I., Kanesaki, Y., Hayashi, H., Hall, J.J., Simon, W.J., Slabas, A.R., and Murata, N., The Histidine Kinase Hik34 Is Involved in Thermotolerance by Regulating the Expression of Heat Shock Genes in Synechocystis, Plant Physiol., 2005, vol. 138, pp. 1409–1421.

    PubMed  Article  CAS  Google Scholar 

  67. 67.

    Shoumskaya, M.A., Paithoonrangsarid, K., Kanesaki, Y., Los, D.A., Zinchenko, V.V., Tanticharoen, M., Suzuki, I., and Murata, N., Identical Hik-Rre Systems Are Involved in Perception and Transduction of Salt Signals and Hyperosmotic Signals but Regulate the Expression of Individual Genes to Different Extents in Synechocystis, J. Biol. Chem., 2005, vol. 280, pp. 21531–21538.

    PubMed  Article  CAS  Google Scholar 

  68. 68.

    Zheng, M., Aslund, F., and Storz, G., Activation of OxyR Transcription Factor by Reversible Disulfide Bond Formation, Science, 1998, vol. 279, pp. 1718–1721.

    PubMed  Article  CAS  Google Scholar 

  69. 69.

    Triantaphylidès, C., Krischke, M., Hoeberichts, F.A., Ksas, B., Gresser, G., Havaux, M., van Breusegem, F., and Mueller, M.J., Singlet Oxygen Is the Major Reactive Oxygen Species Involved in Photooxidative Damage to Plants, Plant Physiol., 2008, vol. 148, pp. 960–968.

    PubMed  Article  Google Scholar 

  70. 70.

    Fischer, B.B., Krieger-Liszkay, A., Hideg, E., Snyrychová, I., Wiesendanger, M., and Eggen, R.I., Role of Singlet Oxygen in Chloroplast to Nucleus Retrograde Signaling in Chlamydomonas reinhardtii, FEBS Lett., 2007, vol. 581, pp. 5555–5560.

    PubMed  Article  CAS  Google Scholar 

  71. 71.

    Scarpeci, T.E., Zanor, M.I., Carrillo, N., Mueller-Roeber, B., and Valle, E.M., Generation of Superoxide Anion in Chloroplasts of Arabidopsis thaliana during Active Photosynthesis: A Focus on Rapidly Induced Genes, Plant Mol. Biol., 2008, vol. 66, pp. 361–378.

    PubMed  Article  CAS  Google Scholar 

  72. 72.

    Rizhsky, L., Liang, H., and Mittler, R., The Water-Water Cycle Is Essential for Chloroplast Protection in the Absence of Stress, J. Biol. Chem., 2003, vol. 278, pp. 38921–38925.

    PubMed  Article  CAS  Google Scholar 

  73. 73.

    Sagi, M. and Fluhr, R., Production of Reactive Oxygen Species by Plant NADPH Oxidases, Plant Physiol., 2006, vol. 141, pp. 336–340.

    PubMed  Article  CAS  Google Scholar 

  74. 74.

    Gadjev, I., Vanderauwera, S., Gechev, T.S., Laloi, C., Minkov, I.N., Shulaev, V., Apel, K., Inze, D., Mittler, R., and van Breusegem, F., Transcriptomic Footprints Disclose Specificity of Reactive Oxygen Species Signaling in Arabidopsis, Plant Physiol., 2006, vol. 141, pp. 436–445.

    PubMed  Article  CAS  Google Scholar 

  75. 75.

    Kovtun, Y., Chiu, W.L., Tena, G., and Sheen, J., Functional Analysis of Oxidative Stress-Activated Mitogen-Activated Protein Kinase Cascade in Plants, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 2940–2945.

    PubMed  Article  CAS  Google Scholar 

  76. 76.

    Nishiyama, Y., Yamamoto, H., Allakhverdiev, S.I., Inaba, M., Yokota, A., and Murata, N., Oxidative Stress Inhibits the Repair of Photodamage to the Photosynthetic Machinery, EMBO J., 2001, vol. 20, pp. 5587–5594.

    PubMed  Article  CAS  Google Scholar 

  77. 77.

    Gupta, R. and Luan, S., Redox Control of Protein Tyrosine Phosphatases and Mitogen-Activated Protein Kinases in Plants, Plant Physiol., 2003, vol. 132, pp. 1149–1152.

    PubMed  Article  CAS  Google Scholar 

  78. 78.

    Rentel, M.C., Lecourieux, D., Ouaked, F., Usher, S.L., Petersen, L., Okamoto, H., Knight, H., Peck, S.C., Grierson, C.S., Hirt, H., and Knight, M.R., OXI1 Kinase Is Necessary for Oxidative Burst-Mediated Signaling in Arabidopsis, Nature, 2004, vol. 427, pp. 858–861.

    PubMed  Article  CAS  Google Scholar 

  79. 79.

    Joo, J.H., Wang, S., Chen, J.G., Jones, A.M., and Fedoroff, N.V., Different Signaling and Cell Death Roles of Heterotrimeric G-Protein α and β Subunits in the Arabidopsis Oxidative Stress Response to Ozone, Plant Cell, 2005, vol. 17, pp. 957–970.

    PubMed  Article  CAS  Google Scholar 

  80. 80.

    Gidrol, X., Sabelli, P.A., Fern, Y.S., and Kush, A.K., Annexin-Like Protein from Arabidopsis thaliana Rescues ΔoxyR Mutant of Escherichia coli from H2O2 Stress, Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 11 268–11 273.

    Article  CAS  Google Scholar 

  81. 81.

    Liu, H., Colavitti, R., Rovira, I.I., and Finkel, T., Redox-Dependent Transcriptional Regulation, Circul. Res., 2005, vol. 97, pp. 967–974.

    Article  CAS  Google Scholar 

  82. 82.

    Neill, S.J., Desikan, R., Clarke, A., Hurst, R.D., and Hancock, J.T., Hydrogen Peroxide and Nitric Oxide as Signalling Molecules in Plants, J. Exp. Bot., 2002, vol. 53, pp. 1237–1247.

    PubMed  Article  CAS  Google Scholar 

  83. 83.

    Kim, M.C., Chung, W.S., Yun, D., and Cho, M.J., Calcium and Calmodulin-Mediated Regulation of Gene Expression in Plants, Mol. Plant., 2009, vol. 2, pp. 13–21.

    PubMed  Article  CAS  Google Scholar 

  84. 84.

    Yin, D., Kuczera, K., and Squier, T.C., The Sensitivity of Carboxyl-Terminal Methionines in Calmodulin Isoforms to Oxidation by H2O2 Modulates the Ability to Activate the Plasma Membrane Ca-ATPase, Chem. Res. Toxicol., 2000, vol. 13, pp. 103–110.

    PubMed  Article  CAS  Google Scholar 

  85. 85.

    Jung, J.-Y., Shin, R., and Schachtaman, D.P., Ethylene Mediates Response and Tolerance to Potassium Deprivation in Arabidopsis, Plant Cell, 2009, vol. 21, pp. 607–621.

    PubMed  Article  CAS  Google Scholar 

  86. 86.

    Munnik, T., Irvine, R.F., and Musgrave, A., Phospholipid Signaling in Plants, Biochim. Biophys. Acta, 1998, vol. 1389, pp. 222–272.

    PubMed  CAS  Google Scholar 

  87. 87.

    Tognetti, V.B., Mühlenbock, P., and van Breusegem, F., Stress Homeostasis—the Redox and Auxin Perspective, Plant Cell Environ., 2011, doi 10.1111/j.1365-3040.2011.02324x

  88. 88.

    Sang, Y., Cui, D., and Wang, X., Phospholipase D and Phosphatidic Acid-Mediated Generation of Superoxide in Arabidopsis, Plant Physiol., 2001, vol. 126, pp. 1449–1458.

    PubMed  Article  CAS  Google Scholar 

  89. 89.

    Dmitriev, A.P., Signal Molecules for Plant Defense Responses to Biotic Stress, Russ. J. Plant Physiol., 2003, vol. 50, pp. 417–425.

    Article  CAS  Google Scholar 

  90. 90.

    Horváth, E., Janda, T., Szalai, G., and Páldi, E., In Vitro Salicylic Acid Inhibition of Catalase Activity in Maize: Differences between the Isozymes and a Possible Role in the Induction of Chilling Tolerance, Plant Sci., 2002, vol. 163, pp. 1129–1135.

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to V. D. Kreslavski.

Additional information

Original Russian Text © V.D. Kreslavski, D.A. Los, S.I. Allakhverdiev, Vl.V. Kuznetsov, 2012, published in Fiziologiya Rastenii, 2012, Vol. 59, No. 2, pp. 163–178.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kreslavski, V.D., Los, D.A., Allakhverdiev, S.I. et al. Signaling role of reactive oxygen species in plants under stress. Russ J Plant Physiol 59, 141–154 (2012). https://doi.org/10.1134/S1021443712020057

Download citation

Keywords

  • plants
  • reactive oxygen species
  • stress
  • signaling system
  • chloroplast