Skip to main content
SpringerLink
Log in

Signal mediators in plants in response to abiotic stress: Calcium, reactive oxygen and nitrogen species

  • Published:
Cytology and Genetics Aims and scope Submit manuscript

Abstract

Perception of signals to abiotic stressors by plant cells is accompanied by an increase in the cytosolic calcium concentration, content of reactive oxygen species (ROS) and nitrogen monoxide (NO) which execute the role of signal mediators at the activation of gene expression responsible for defense responses. Calcium ions, ROS, and NO stay in the multiple functional interactions, which provide intensifying and transduction of signals into the genetic apparatus and the signal attenuation. Increased content of at least one of these signal mediators in the cells may cause the activation of a number of signaling cascades and the formation of plant adaptive reactions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Kaur, N. and Gupta, A.K., Signal transduction pathways under abiotic stresses in plant, Curr. Sci., 2005, vol. 88, pp. 1771–1780.

    CAS  Google Scholar 

  2. Jeandroz, S., Lamotte, O., Astier, J., et al., There’s more to the picture than meets the eye: nitric oxide cross talk with Ca2+ signaling, Plant Physiol., 2013, vol. 163, pp. 459–470.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Tuteja, N. and Sopory, S.K., Chemical signaling under abiotic stress environment in plants, Plant Signal. Behav., 2008, vol. 3, pp. 525–536.

    Article  PubMed Central  PubMed  Google Scholar 

  4. 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Medvedev, S.S., Calcium signaling system in plants, Russ. J. Plant Physiol., 2005, vol. 52, no. 2, pp. 249–270.

    Article  CAS  Google Scholar 

  6. Tarchevskii, I.A., Signal’nye sistemy kletok rastenii (Signal Systems of Plant Cells), Moscow: Nauka, 2002.

    Google Scholar 

  7. Johnson, J.M., Reichelt, M., Vadassery, J., et al., An Arabidopsis mutant impaired in intracellular calcium elevation is sensitive to biotic and abiotic stress, BMC Plant Biol., 2014, vol. 1, p. 162.

    Article  CAS  Google Scholar 

  8. Demidchik, V., Davenport, R.J., and Tester, M.A., Nonselective cation channels in plants, Annu. Rev. Plant Biol., 2002, vol. 53, pp. 67–107.

    Article  CAS  PubMed  Google Scholar 

  9. Krutetskaya, Z.I. and Lebedev, O.E., Mechanisms of Ca2+ signaling in cells, Tsitologiya, 2001, vol. 43, no. 1, pp. 5–32.

    CAS  Google Scholar 

  10. Lecourieux, D., Mazars, C., Pauly, N., et al., Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells, Plant Cell, 2002, vol. 14, pp. 2627–2641.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Allen, G.J., Muir, S.R., and Sanders, D., Release of Ca2+ from individual plant vacuoles by both InsP3 and cyclic ADP-ribose, Science, 1995, vol. 268, pp. 735–737.

    Article  CAS  PubMed  Google Scholar 

  12. Chin, K., Moeder, W., and Yoshioka, K., Biological roles of cyclic-nucleotide-gated ion channels in plants: what we know and don’t know about this 20 member ion channel family, Botany, 2009, vol. 87, no. 7, pp. 668–677.

    Article  CAS  Google Scholar 

  13. Gimalov, F.R., Baymiev, A.Kh., Matniyazov, R.T., et al., Initial stages of low-temperature induction of cabbage cold shock protein gene csp5, Biochemistry (Moscow), 2004, vol. 69, no. 5, pp. 575–579.

    Article  CAS  Google Scholar 

  14. Finka, A. and Goloubinoff, P., The CNGCb and CNGCd genes from Physcomitrella patens moss encode for thermosensory calcium channels responding to fluidity changes in the plasma membrane, Cell Stress Chaperones, 2014, vol. 19, pp. 83–90.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Drobak, B.K. and Watkins, P.A.C., Inositol(1,4,5)trisphosphate production in plant cells: an early response to salinity and hyperosmotic stress, FEBS Lett., 2000, vol. 481, pp. 240–244.

    Article  CAS  PubMed  Google Scholar 

  16. Liu, H.T., Huang, W.D., Pan, Q.H., et al., Contributions of PiP2-specific-phospholipase C and free salicylic acid to heat acclimation-induced thermotolerance in pea leaves, J. Plant Physiol., 2006, vol. 163, pp. 405–416.

    Article  CAS  PubMed  Google Scholar 

  17. Hepler, P.K., Calcium: a central regulator of plant growth and development, Plant Cell, 2005, vol. 17, pp. 2142–2155.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Gimalov, F.R., Chemeris, A.V., and Vakhitov, V.A., Perception of the cold signal by plant, Usp. Sovrem. Biol., 2004, vol. 124, no. 2, pp. 185–196.

    CAS  Google Scholar 

  19. Chin, D. and Means, A.R., Calmodulin: a prototypical calcium sensor, Trends Cell. Biol., 2000, vol. 10, pp. 322–328.

    Article  CAS  PubMed  Google Scholar 

  20. Ranty, B., Aldon, D., and Galaud, J.P., Plant calmodulins and calmodulin-related proteins: multifaceted relays to decode calcium signals, Plant Signal. Behav., 2006, vol. 1, no. 3, pp. 96–104.

    Article  PubMed Central  PubMed  Google Scholar 

  21. Pardo, J.M., Reddy, M.P., Yang, S., et al., Stress signaling through Ca2+/calmodulin-dependent protein phosphatase calcineurin mediates salt adaptation in plants, Proc. Nat. Acad. Sci. USA, 1998, vol. 95, pp. 9681–9686.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Albrecht, V., Weinl, S., Blazevic, D., et al., The calcium sensor cbl1 integrates plant responses to abiotic stresses, Plant J., 2003, vol. 36, pp. 457–470.

    Article  CAS  PubMed  Google Scholar 

  23. Chinnusamy, C., Schumaker, K., and Zhu, J.K., Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants, J. Exp. Bot., 2004, vol. 55, pp. 225–236.

    Article  CAS  PubMed  Google Scholar 

  24. Larkindale, J. and Huang, B., Thermotolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene, J. Plant Physiol., 2004, vol. 161, pp. 405–413.

    Article  CAS  PubMed  Google Scholar 

  25. Hu, X., Jiang, M., Zhang, J., et al., Calcium-calmodulin is required for abscisic acid-induced antioxidant defense and functions both upstream and downstream of H2O2 production in leaves of maize (Zea mays) plants, New Phytol., 2007, vol. 173, pp. 27–38.

    Article  CAS  PubMed  Google Scholar 

  26. Ma, S.Y. and Zhao, M., Calcium regulation of Arabidopsis salt resistance, Acta Agron Sin, 2006, vol. 32, no. 11, pp. 1706–1711.

    CAS  Google Scholar 

  27. Yang, Y., Yang, F., Li, X., et al., Signal regulation of praline metabolism in callus of the halophyte Nitraria tangutorum Bobr. grown under salinity stress, Plant Cell, Tiss. Org. Cult., 2013, vol. 112, no. 1, pp. 33–42.

    Article  CAS  Google Scholar 

  28. Trofimova, M.S., Andreev, I.M., and Kuznetsov, V.V., Calcium is involved in regulation of the synthesis of hsps in suspension-cultured sugar beet cell sunder hyperthermia, Physiol. Plant., 1999, vol. 105, pp. 67–73.

    Article  CAS  Google Scholar 

  29. Li, B., Liu, H.T., Sun, D.Y., and Zhou, R.G., Ca2+ and calmodulin modulate DNA-binding activity of maize heat shock transcription factor in vitro, Plant Cell Physiol., 2004, vol. 45, pp. 627–634.

    Article  CAS  PubMed  Google Scholar 

  30. Scandalios, J.G., The rise of ROS, Trends Biochem. Sci., 2002, vol. 27, pp. 483–486.

    Article  CAS  PubMed  Google Scholar 

  31. Pitzschke, A. and Hirt, H., Mitogen-activated protein kinases and reactive oxygen species signaling in plants, Plant Physiol., 2006, vol. 141, pp. 351–356.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Sagi, M. and Fluhr, R., Production of reactive oxygen species by plant NADPH oxidases, Plant Physiol., 2006, vol. 141, pp. 336–340.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Kreslavski, V.D., Los, D.A., Allakhverdiev, S.I., and Kuznetsov, Vl.V., Signaling role of reactive oxygen species in plants under stress, Russ. J. Plant Physiol., 2012, vol. 59, no. 2, pp. 141–154.

  34. Foyer, C.H. and Noctor, G., Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications, Antioxid. Redox Signal., 2009, vol. 11, pp. 861–906.

    Article  CAS  PubMed  Google Scholar 

  35. Foyer, C.H. and Shigeoka, S., Understanding oxidative stress and antioxidant functions to enhance photosynthesis, Plant Physiol., 2011, vol. 155, pp. 93–100.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Lee, K.P., Kim, C., Landgraf, F., and Apel, K., EXECUTER1and 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. 10270–10275.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Rhoads, D.M., Umbach, A.L., Subbaiah, C.C., and Siedow, J.N., Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling, Plant Physiol., 2006, vol. 141, pp. 357–366.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Cvetkovska, M. and Vanlerberghe, G.C., Alternative oxidase impacts the plant response to biotic stress by influencing the mitochondrial generation of reactive oxygen species, Plant, Cell Environ., 2013, vol. 36, pp. 721–732.

    Article  CAS  Google Scholar 

  39. Purvis, A.C., Role of the alternative oxidase in limiting superoxide production by plant mitochondria, Physiol. Plant., 1997, vol. 100, pp. 165–170.

    Article  CAS  Google Scholar 

  40. Dmitriv, O.P. and Kravchuk, Zh.M., Reactive oxygen species and immunity of plants, Tsitol. Genet., 2005, vol. 39, no. 4, pp. 64–75.

    Google Scholar 

  41. Piotrovskii, M.S., Shevyreva, T.A., Zhestkova, I.M., and Trofimova, M.S., Activation of plasmalemmal NADPH oxidase in etiolated maize seedlings exposed to chilling temperatures, Russ. J. Plant Physiol., 2011, vol. 58, pp. 290–298.

    Article  CAS  Google Scholar 

  42. Kolupaev, Yu.E., Oboznyi, A.I., and Shvidenko, N.V., Role of hydrogen peroxide in generation of a signal inducing heat tolerance of wheat seedlings, Russ. J. Plant Physiol., 2013, vol. 62, no. 2, pp. 227–234.

    Article  CAS  Google Scholar 

  43. Jaspers, P. and Kangasjarvi, J., Reactive oxygen species in abiotic stress signaling, Physiol. Plant., 2010, vol. 138, pp. 405–413.

    Article  CAS  PubMed  Google Scholar 

  44. Gupta, D.K., Inouhe, M., Serrano, M., et al., Oxidative stress and arsenic toxicity: role of NADPH oxidases, Chemosphere, 2013, vol. 90, pp. 1987–1996.

    Article  CAS  PubMed  Google Scholar 

  45. Bailey-Serres, J. and Chang, R., Sensing and signaling in response to oxygen deprivation in plants and other organisms, Ann. Bot., 2005, vol. 96, pp. 507–518.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Mittler, R., Vanderauwera, S., Suzuki, N., et al., ROS signaling: the new wave?, Trends Plant Sci., 2011, vol. 16, pp. 300–309.

    Article  CAS  PubMed  Google Scholar 

  47. Mori, I.C. and Schroeder, J.S., 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Kwak, J.M., Nguyen, V., and Schroeder, J.I., The role of reactive oxygen species in hormonal responses, Plant Physiol., 2006, vol. 141, pp. 323–329.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Wong, H.L., Pinontoan, R., Hayashi, K., et al., Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension, Plant Cell, 2007, vol. 19, pp. 4022–4034.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  50. Ogasawara, Y., Kaya, H., Hiraoka, G., et al., Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation, J. Biol. Chem., 2008, vol. 283, pp. 8885–8892.

    Article  CAS  PubMed  Google Scholar 

  51. Sagi, M. and Fluhr, R., Superoxide production by plant homologues of the gp91phox NADPH oxidase: modulation of activity by calcium and by tobacco mosaic virus infection, Plant Physiol., 2001, vol. 126, pp. 1281–1290.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  52. Oda, T., Hashimoto, H., Kuwabara, N., et al., Structure of the N-terminal regulatory domain of a plant NADPH oxidase and its functional implications, J. Biol. Chem., 2010, vol. 285, pp. 1435–1445.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  53. Neill, S.J., Desikan, R., Clarke, A., et al., Hydrogen peroxide and nitric oxide as signaling molecules in plants, J. Exp. Bot., 2002, vol. 53, pp. 1237–1247.

    Article  CAS  PubMed  Google Scholar 

  54. Misra, S., Wu, Y., Venkataraman, G., et al., Heterotrimeric G-protein complex and G-protein-coupled receptor from a legume (Pisum sativum): role in salinity and heat stress and cross-talk with phospholipase C Plant J., 2007, vol. 51, pp. 656–669.

    Article  CAS  PubMed  Google Scholar 

  55. Szalai, G., Kellos, T., Galiba, G., and Kocsy, G., Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions, J. Plant Growth Regul., 2009, vol. 28, pp. 66–80.

    Article  CAS  Google Scholar 

  56. Noctor, G., Gomez, L., Vanacker, H., and Foyer, C.H., Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling, J. Exp. Bot., 2002, vol. 53, pp. 1283–1304.

    Article  CAS  PubMed  Google Scholar 

  57. Georgiou, C.D., Patsoukis, N., Papapostolou, I., and Zervoudakis, G., Sclerotial metamorphosis in filamentous fungi is induced by oxidative stress, Integr. Comr. Biol., 2006, vol. 46, pp. 691–712.

    Article  CAS  Google Scholar 

  58. Mazid, M., Ahmed, K.T., and Mohammad, F., Role of nitric oxide in regulation of H2O2 mediating tolerance of plants to abiotic stress: a synergistic signaling approach, J. Stress Physiol. Biochem., 2011, vol. 7, no. 2, pp. 34–74.

    Google Scholar 

  59. Vranova, E., Inze, D., and Breusegem, F., Signal transduction during oxidative stress, J. Exp. Bot., 2002, vol. 53, pp. 1227–1236.

    Article  CAS  PubMed  Google Scholar 

  60. Mur, L.A.J., Kenton, P., Atzorn, R., et al., The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death, Plant Physiol., 2006, vol. 140, pp. 249–262.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  61. Ndamukong, I., Al Abdallat, A., Thurow, C., et al., SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA responsive PDF1.2 transcription, Plant J., 2007, vol. 50, pp. 128–139.

    Article  CAS  PubMed  Google Scholar 

  62. Mou, Z., Fan, W., and Dong, X., Inducers of plant systemic acquired resistance regulate npr1 function through redox changes, Cell, 2003, vol. 113, pp. 935–944.

    Article  CAS  PubMed  Google Scholar 

  63. Divi, U.K., Rahman, T., and Krishna, P., Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways, BMC Plant Biol., 2010, vol. 10, pp. 151–164.

    Article  PubMed  CAS  Google Scholar 

  64. Pulido, P., Dominguez, F., and Cejudo, F.J., A hydrogen peroxide detoxification system in the nucleus of wheat seed cells. Protection or signaling role?, Plant Signal. Behav., 2009, vol. 4, pp. 23–25.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  65. Wahid, A. and Close, T.J., Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves, Biol. Plant., 2007, vol. 51, pp. 104–109.

    Article  CAS  Google Scholar 

  66. Chaneva, G., Tzanova, A., and Uzunova, A., Interaction between cadmium and paraquat stress on Pisum sativum. Oxidative stress in pea plants induced by Cd2+ and paraquat, Dokl. Blg. AN, 2006, vol. 59, pp. 657–662.

    CAS  Google Scholar 

  67. Bartoli, C.G., Casalongueb, C.A., SImontacchia, M., et al., Interactions between hormone and redox signaling pathways in the control of growth and cross tolerance to stress, Environ. Exp. Bot., 2013, vol. 94, pp. 73–88.

    Article  CAS  Google Scholar 

  68. Kolupaev, Yu.E., Yastreb, T.O., Shvidenko, N.V., and Karpets, Yu.V., Induction of heat resistance of wheat coleoptiles by salicylic and succinic acids: connection of the effect with the generation and neutralization of reactive oxygen species, Appl. Biochem. Microbiol., 2012, vol. 48, no. 5, pp. 500–505.

    Article  CAS  Google Scholar 

  69. Kolupaev, Yu.E., Vainer, A.A., Yastreb, T.O., et al., The role of reactive oxygen species and calcium ions in the implementation of the stress-protective effect of brassinosteroids on plant cells, Appl. Biochem. Microbiol., 2014, vol. 50, no. 6, pp. 658–663.

    Article  CAS  Google Scholar 

  70. Wilson, I.D., Neill, S.J., and Hancock, J.T., Nitric oxide synthesis and signaling in plants, Plant, Cell Environ., 2008, vol. 31, pp. 622–631.

    Article  CAS  Google Scholar 

  71. Neill, S., Bright, J., Desikan, R., et al., Nitric oxide evolution and perception, J. Exp. Bot., 2008, vol. 59, pp. 25–35.

    Article  CAS  PubMed  Google Scholar 

  72. Glyan’ko, A.K. and Mitanova, N.B., The synthesis of nitric oxide (NO) in the roots of etiolated pea seedlings, Visn. Kharkiv. Nats. Agrar. Univ., Ser. Biol., 2011, vol. 3, no. 24, pp. Ñ. 6–14..

    Google Scholar 

  73. Ludidi, N. and Gehring, C., Identification of a novel protein with guanylyl cyclase activity in Arabidopsis thaliana, J. Biol. Chem., 2003, vol. 278, pp. 6490–6494.

    Article  CAS  PubMed  Google Scholar 

  74. Bakakina, Yu.S., Kolesneva, E.V., Dubovskaya, L.V., and Volotovskii, I.D., Effect of high-temperature stress on the intracellular concentration of NO and endogenous cGMP content in Arabidopsis thaliana seedlings, Vestsi Nats. Akad. Navuk Belarusi. Ser Biyal. Navuk, 2011, no. 1, pp. 50–56.

    Google Scholar 

  75. Lamotte, O., Guold, K., Lecourieux, D., et al., Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein, Plant Physiol., 2004, vol. 135, pp. 516–529.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  76. Krasilenko, Yu.A., Yemets, A.I., and Blume, Ya.B., Functional role of nitric oxide in plants, Russ. J. Plant Physiol., 2010, vol. 57, pp. 451–461.

    Article  CAS  Google Scholar 

  77. Zhang, Y., Wang, L., Liu, Y., et al., Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast, Planta, 2006, vol. 224, pp. 545–555.

    Article  CAS  PubMed  Google Scholar 

  78. Krasylenko, Ya.., Yemets, A.I., Sheremet, Ya.., and Blume, Ya.B., Nitric oxide as a critical factor for perception of UV-B irradiation by microtubules in Arabidopsis, Physiol. Plant., 2012, vol. 145, pp. 505–515.

    Article  CAS  PubMed  Google Scholar 

  79. Santa-Cruz, D.M., Pacienza, N.A., Polizio, A.H., et al., Nitric oxide synthase-like dependent no production enhances heme oxygenase up-regulation in ultraviolet-B-irradiated soybean plants, Phytochemistry, 2010, vol. 71, pp. 1700–1707.

    Article  CAS  PubMed  Google Scholar 

  80. Siddiqui, M.H., Al-Whaibi, M.H., and Basalah, M.O., Role of nitric oxide in tolerance of plants to abiotic stress, Protoplasma, 2011, vol. 248, pp. 447–455.

    Article  CAS  PubMed  Google Scholar 

  81. Uchida, A., Jagendorf, A.T., Hibino, T., et al., Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice, Plant Sci., 2002, vol. 163, pp. 515–523.

    Article  CAS  Google Scholar 

  82. Chzhan, Kh., Li, Ya.Kh., Khu, L.Yu., et al., Vliyanie obrabotki list’ev pshenitsy donorom okisi azota na antiokislitel’nyi metabolizm pri stresse, vyzvannom alyuminiem, Fiziol. Rastenii, 2008, vol. 54, no. 4, pp. 523–528.

    Google Scholar 

  83. Vital, S.A., Fowler, R.W., Virgen, A., et al., Opposing roles for superoxide and nitric oxide in the NaCl stress-induced upregulation of antioxidant enzyme activity in cotton callus tissue, Environ. Exp. Bot., 2008, vol. 62, pp. 60–68.

    Article  CAS  Google Scholar 

  84. Talukdar, D., Arsenic-induced oxidative stress in the common bean legume, Phaseolus vulgaris L. seedlings and its amelioration by exogenous nitric oxide, Physiol. Mol. Biol. Plants, 2013, vol. 19, pp. 69–79.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  85. Baxter, A., Mittler, R., and Suzuki, N., ROS as key players in plant stress signaling, J. Exp. Bot., 2013, vol. 65, pp. 1229–1240.

    Article  PubMed  CAS  Google Scholar 

  86. Courtois, C., Besson, A., Dehan, J., et al., Nitric oxide signaling in plants: interplays with Ca2+ and protein kinases, J. Exp. Bot., 2008, vol. 59, pp. 155–163.

    Article  CAS  PubMed  Google Scholar 

  87. Richards, S.L., Laohavisit, A., Mortimer, J.C., et al., Annexin 1 regulates the H2O2-induced calcium signature in Arabidopsis thaliana roots, Plant J., 2014, vol. 77, pp. 136–145.

    Article  CAS  PubMed  Google Scholar 

  88. Zhang, A., Jiang, M., Zhang, J., et al., Nitric oxide induced by hydrogen peroxide mediates abscisic acidinduced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves, New Phytol., 2007, vol. 175, pp. 36–50.

    Article  CAS  PubMed  Google Scholar 

  89. Dubovskaya, L.V., Bakakina, Y.S., Kolesneva, E.V., et al., cGMP-dependent ABA-induced stomatal closure in the ABA-insensitive Arabidopsis mutant abi1-1, New Phytol., 2011, vol. 191, pp. 57–69.

    Article  CAS  PubMed  Google Scholar 

  90. Laxalt, A.M., Raho, N., Ten, Have, A., and Lamattina, L., Nitric oxide is critical for inducing phosphatidic acid accumulation in xylanase-elicited tomato cells, J. Biol. Chem., 2007, vol. 282, pp. 21160–21168.

    Article  CAS  PubMed  Google Scholar 

  91. Klausner, R.D., Rouault, T.A., and Harford, J.B., Regulating the fate of mRNA: the control of cellular iron metabolism, Cell, 1993, vol. 72, pp. 19–28.

    Article  CAS  PubMed  Google Scholar 

  92. Lanteri, M.L., Laxalt, A.M., and Lamattina, L., Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in cucumber, Plant Physiol., 2008, vol. 147, pp. 188–198.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  93. Yun, B.W., Feechan, A., Yin, M., et al., S-nitrosylation of NADPH oxidase regulates cell death in plant immunity, Nature, 2011, vol. 478, pp. 264–268.

    Article  CAS  PubMed  Google Scholar 

  94. Konopka-Postupolska, D., Clark, G., Goch, G., et al., The role of annexin 1 in drought stress in Arabidopsis, Plant Physiol., 2009, vol. 150, pp. 1394–1410.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  95. Laohavisit, A., Brown, A.T., Cicuta, P., and Davies, J.M., Annexins: components of the calcium and reactive oxygen signaling network, Plant Physiol., 2010, vol. 152, pp. 1824–1829.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  96. Kolupaev, Yu.E., Akinina, G.E., and Mokrousov, A.V., Induction of heat tolerance in wheat coleoptiles by calcium ions and its relation to oxidative stress, Russ. J. Plant Physiol., 2005, vol. 52, no. 2, pp. 199–204.

    Article  CAS  Google Scholar 

  97. Kolupaev, Yu.Ye., Karpets, Yu.V., and Kosakivska, I.V., The importance of reactive oxygen species in the induction of plant resistance to heat stress, Gen. Appl. Plant Physiol., 2008, vol. 34, nos. 3/4, pp. 251–266.

    CAS  Google Scholar 

  98. Karpets, Yu.V. and Kolupaev, Yu.E., The peroxide content in the roots of wheat seedlings in hyperthermia depending on the calcium status of their cella, Visn. Kharkiv. Nats. Agrar. Univ., Ser. Biol., 2008, vol. 3, no. 15, pp. 33–40.

    Google Scholar 

  99. Xu, M.J., Dong, J.F., and Zhang, X.B., Signal interaction between nitric oxide and hydrogen peroxide in heat shock-induced hypericin production of Hypericum perforatum suspension cells, Sci. China. Ser. C: Life Sci., 2008, vol. 51, pp. 676–686.

    Article  CAS  Google Scholar 

  100. Karpets, Yu.V., Kolupaev, Yu.E., and Vainer, A.A., Functional interaction between nitric oxide and hydrogen peroxide during formation of wheat seedling induced heat resistance, Russ. J. Plant Physiol., 2015, vol. 62, no. 1, pp. 65–70.

    Article  CAS  Google Scholar 

  101. Pasqualini, S., Meier, S., Gehring, C., et al., Ozone and nitric oxide induce cGMP-dependent and -independent transcription of defense genes in tobacco, New Phytol., 2009, vol. 181, pp. 860–870.

    Article  CAS  PubMed  Google Scholar 

  102. Lu, D., Zhang, X., Juang, J., et al., No may function in the downstream of H2O2 in ABA-induced stomatal closure in Vicia faba L., J. Plant Physiol. Mol. Biol., 2005, vol. 31, pp. 62–70.

    Google Scholar 

  103. Tewari, R.K., Hahn, E.J., and Paek, K.Y., Function of nitric oxide and superoxide anion in the adventitious root development and antioxidant defense in Panax ginseng, Plant Cell Rep., 2008, vol. 27, pp. 563–573.

    Article  CAS  PubMed  Google Scholar 

  104. Karpets, Yu.V., Kolupaev, Yu.E., and Yastreb, T.O., Effect of sodium nitroprusside on heat resistance of wheat coleoptiles: dependence on the formation and scavenging of reactive oxygen species, Russ. J. Plant Physiol., 2011, vol. 58, no. 6, pp. 1027–1033.

    Article  CAS  Google Scholar 

  105. Marino, D., Dunand, C., Puppo, A., and Pauly, N., A burst of plant NADPH oxidases, Trends Plant Sci., 2012, vol. 17, pp. 9–15.

    Article  CAS  PubMed  Google Scholar 

  106. Karpets, Yu.V., Kolupaev, Yu.E., Yastreb, T.O., and Dmitriev, O.P., Possible pathways of heat resistance induction in plant cells by exogenous nitrogen oxide, Cytol. Genet., 2012, vol. 46, no. 6, pp. 354–359.

    Article  Google Scholar 

  107. Reiter, C.D., Teng, R.J., and Beckman, J., Superoxide reacts with nitric oxide to nitrate tyrosine at physiological ph via peroxynitrite, J. Biol. Chem., 2000, vol. 275, pp. 32460–32466.

    Article  CAS  PubMed  Google Scholar 

  108. Dubovskaya, L.V., Kolesneva, E.V., Knyazev, D.M., and Volotovskii, I.D., Protective role of nitric oxide during hydrogen peroxide-induced oxidative stress in tobacco plants, Russ. J. Plant Physiol., 2007, vol. 56, no. 6, pp. 755–762.

    Article  CAS  Google Scholar 

  109. Dmitriev, A.P., Signaling role of nitric oxide in plants, Tsitol. Genet., 2004, vol. 38, no. 4, pp. 67–75.

    CAS  PubMed  Google Scholar 

  110. Glyan’ko, A.K., Ishchenko, A.A., and Stepanov, A.V., Influence of calcium and rhizobial infections (Rhizobium leguminosarum) on the dynamics of nitric oxide (NO) content in roots of etiolated pea (Pisum sativum L.) seedlings, Appl. Biochem. Microbiol., 2014, vol. 56, no. 6, pp. 652–657.

    Article  CAS  Google Scholar 

  111. Besson-Bard, A., Pugin, A., and Wendehenne, D., New insights into nitric oxide signaling in plants, Annu. Rev. Plant Biol., 2008, vol. 59, pp. 21–39.

    Article  CAS  PubMed  Google Scholar 

  112. Moller, I.M. and Sweetlove, L.J., ROS signaling-specificity is required, Trends Plant Sci., 2010, vol. 15, pp. 370–374.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dokuchaev Kharkov National Agrarian University, Kharkov, Ukraine

    Yu. E. Kolupaev & Yu. V. Karpets

  2. Institute of Cell Biology and Genetic Engineering, National Academy of Sciences of Ukraine, Kiev, Ukraine

    A. P. Dmitriev

Authors
  1. Yu. E. Kolupaev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu. V. Karpets
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. P. Dmitriev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yu. E. Kolupaev.

Additional information

Original Russian Text © Yu.E. Kolupaev, Yu.V. Karpets, A.P. Dmitriev, 2015, published in Tsitologiya i Genetika, 2015, Vol. 49, No. 5, pp. 73–86.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kolupaev, Y.E., Karpets, Y.V. & Dmitriev, A.P. Signal mediators in plants in response to abiotic stress: Calcium, reactive oxygen and nitrogen species. Cytol. Genet. 49, 338–348 (2015). https://doi.org/10.3103/S0095452715050047

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0095452715050047

Keywords

Search

Navigation