Visn. Hark. nac. agrar. univ., Ser. Biol., 2017, Issue 2 (41), с. 6-31


Yu. V. Karpets1, Yu. E. Kolupaev1, 2

1V.V. Dokuchaev Kharkiv National Agrarian University
(Kharkiv, Ukraine)
2V.N. Karazin Kharkiv National University
(Kharkiv, Ukraine)

In the review the literary and own data on the change of content of endogenous nitric oxide in plants at adaptation and influence of nitric oxide donors on resistance to abiotic stressors are analysed and generalized. The role of nitrate reductase, animals NO-synthase-like enzyme, and other euzymatic systems in the NO production in plant cells, and also the interaction of various pathways of nitric oxide synthesis is discussed. The role of calcium and reactive oxygen species (ROS) in the regulation of activity of NO-generating enzymes is analysed. The influence of nitric oxide on calcium homeostasis, and also on processes of generation and neutralization of ROS in plant cells is considered. The special attention is paid to the role of S-nitrosylation, nitration on tyrosine and nitrosylations of metals in the regulation of antioxidant enzymes activity. Data on functional interaction of NO with other signaling mediators at the transduction of stress phytohormones signals are provided. The conclusion about the central role of nitric oxide in the functioning of difficult signaling network in plant cells is made.

Key words: nitric oxide, nitrate reductase, animals NO-synthase-like enzyme, calcium, reactive oxygen species, signaling, antioxidant enzymes, plant adaptive responses



1. Bakakina Y.S., Kolesneva E.V., Dubovskaya L.V., Volotovski I.D. 2009a. Cold stress modulates of NO and cGMP in Arabidopsis thaliana seedlings. Vesti Nats. Akad. Navuk Belarusi. Ser. Biyal. Navuk. 3 : 43-46.
2. Bakakina Y.S., Dubovskaya L.V., Volotovski I.D. 2009b. Heat stress modulated endogenous levels of NO and cGMP in Arabidopsis thaliana seedlings. Vesti Nats. Akad. Navuk Belarusi. Ser. Biyal. Navuk. 4 : 34-39.
3. Bakakina Y.S., Dubovskaya L.V., Volotovski I.D. 2009c.The effect of nitric oxide on the intracellular concentration of calcium ions in transgenic plants Nicotiana plumbaginiflora. Vesti Nats. Akad. Navuk Belarusi. Ser. Biyal. Navuk. 4 : 28-33.
4. Bakakina Y.S., Kolesneva E.V., Dubovskaya L.V., Volotovski I.D. 2011. Nitric oxide and cyclic guanosine 3',5'-monophosphate mediate temperature stresses-induced Ca2+ -responses in Arabidopsis thaliana seedlings. Vesti Nats. Akad. Navuk Belarusi. Ser. Biyal. Navuk. 1 : 50-56.
5. Galeeva E. I., Trifonova T. V., Ponomareva A. A., Viktorova L. V., Minibayeva F. V. 2012. Nitrate reductase from Triticum aestivum leaves: Regulation of activity and possible role in production of nitric oxide. Biochemistry (Mosc.). 77 (4) : 404-410.
6. Glyan'ko A.K., Vasil'eva G.G. 2010. Reactive oxygen and nitrogen species in legume-rhizobial symbiosis: A review. Appl. Biochem.Microbiol. 46 (1) : 15-23.
7. Glyan'ko A.K., Ischenko A.A. 2017. Reactive oxygen and nitrogen species as possible mediators of system resistance in fabaceae affected by rhizobial infection Visn. Hark. nac. agrar. univ., Ser. Biol. 1 (40) : 9-20.
8. Glyan'ko A.K., Mitanova N.B., Stepanov A.V. 2012. Influence of environmental factors on the generation of nitric oxide in the roots of etiolated pea seedlings. Appl. Biochem.Microbiol. 48 (1) : 83-89.
9. Dubovskaya L.V., Kolesneva E.V., Knyazev D.M., Volotovskii I.D. 2007. Protective role of nitric oxide during hydrogen peroxide-induced oxidative stress in tobacco plants. Russ. J. Plant Physiol. 54(6) : 847-855.
10. Karpets Yu.V., Kolupaev Yu.E., Vayner A.A. 2015a. Functional interaction between nitric oxide and hydrogen peroxide during formation of wheat seedling induced heat resistance. Russ. J. Plant Physiol. 62 (1) : 65-70.
11. Karpets Yu.V., Kolupaev Yu.E., Dmitriev A.P. 2017. Induction of NO synthesis in roots of wheat plantlets and development of their heat resistance by exogenous L-arginine and nitrate. Dopov. Nac. acad. nauk Ukr. 7 : 77-84.
12. Karpets Yu.V., Kolupaev Yu.E., Kosakivska I.V. 2016. Nitric oxide and hydrogen peroxide as signal mediators at induction of heat resistance of wheat plantlets by exogenous jasmonic and salicylic acids. Fiziol. rast. genet. 48 (2) : 158-166.
13. Karpets Yu.V., Kolupaev Yu.E., Lugovaya A.A., Oboznyi A.I. 2014a. Effect of jasmonic acid on the pro-/antioxidant system of wheat coleoptiles as related to hyperthermia tolerance. Russ. J. Plant Physiol. 61(3) : 339-346.
14. Karpets Yu.V., Kolupaev Yu.E., Oboznyi O.I., Yastreb T.O. 2015b. Influence of calcium antagonists on generation of reactive oxygen species induced by no donor and development of heat resistance of wheat coleoptiles. Fiziol. rast. genet. 47 (4) : 338-346.
15. Karpets Yu.V., Kolupaev Yu.E., Shvydenko M.V., Lugova G.A. 2014b. Participation of nitric oxide in development of heat resistance of wheat plantlets induced by short-term heating. Visn. Hark. nac. agrar. univ., Ser. Biol. 1 (31) : 47-54.
16. Karpets Yu.V., Kolupaev Yu.E., Shvydenko N.V., Yastreb T.O. 2016b. Induction of heat resistance of plant cells and activation of antioxidant enzymes under influence of nitric oxide depend on changes of calcium homeostasis. Annual meeting of the Society of Plant Physiologists of Russia. Plant signaling systems: from the receptor to the body's response. (June 21-24, 2016, St. Petersburg, Russia St. Petersburg : 331.
17. Karpets Yu.V., Kolupaev Yu.E., Yastreb T.O. 2011. Effect of sodium nitroprusside on heat resistance of wheat coleoptiles: Dependence on the formation and scavenging of reactive oxygen species. Russ. J. Plant Physiol. 58(6) : 1027.
18. Karpets Yu.V., Kolupaev Yu.E., Yastreb T.O., Oboznyi A.I. 2016c. Induction of heat resistance in wheat seedlings by exogenous calcium, hydrogen peroxide, and nitric oxide donor: functional interaction of signal mediators. Russ. J. Plant Physiol. 63 (4) : 490-498.
19. Kolupaev Yu.E. 2016. Plant cell antioxidants and their role in ROS signaling and plant resistance. Uspekhi Sovrem. Biologii. 136 (2) : 181-198.
20. Kolupaev Yu. E., Karpets Yu. V., Yastreb T. O., Lugovaya A. A. 2016. Signal mediators in realization of physiological effects of stress phytohormones. Visn. Hark. nac. agrar. univ., Ser. Biol. 1 (37) : 42-52.
21. Kolupaev Yu.E., Yastreb T.O. 2013. Stress-protective effects of salicylic acid and its structural analogues. Fiziologiys i Biokhimiya Kul't. Rastenii. 45 (2) : 113-126.
22. Kolupaev Yu.E., Yastreb T.O., Shvidenko N.V., Karpets Yu.V. 2012. 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. 48 : (5) : 500-505.
23. Mamaeva A.S., Fomenkov A.A., Nosov A.V., Moshkov I.E., Mur L.A.J., Hall M.A., Novikova G.V. 2015. Regulatory role of nitric oxide in plants. Russ. J. Plant Physiol. 62 (4) : 427-440.
24. Severina I.S. 1998. Role of soluble guanylate cyclase in the molecular mechanism underlying the physiological effects of nitric oxide. Biochemistry (Mosc.). 63 (7) : 939-947.
25. Tarchevskii I.A.. 2002. Plant Cell Signaling Systems. Moscow : 294p.
26. Titov V.Yu., Petrenko Yu.M., Vanin A.F. 2008. Mechanism of inhibition of catalase by nitro and nitroso compounds. Biochemistry (Mosc.). 73 (1) : 92-96.
27. Tian X.R., Lei Y.B. 2007. Physiological responses of wheat seedlings to drought and UV-B radiation. Effect of exogenous sodium nitroprusside application. Russ. J. Plant Physiol. 54 (5) : 676-682.
28. Zhang H., Li Y.H., Hu L.Y., Wang S.H., Zhang F.Q., Hu K.D. 2008. Effects of exogenous nitric oxide donor on antioxidant metabolism in wheat leaves under aluminum stress. Russ. J. Plant Physiol. 55 (4) : 469-474.
29. Yarullina D.R., Smolentseva O.A., Kolpakov A.I., Ilinskaya O.N. 2010. High-temperature stress activates nitric oxide synthesis in Lactobacillus plantarum. Doklady Biological Sciences. 430 (1) : 70-71.
30. Ahmad P., Latef A.A. A., Hashem A., Abd_Allah E.F., Gucel S., Tran L.S.P. 2016. Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front. Plant Sci. 7 : 347. doi: 10.3389/fpls.2016.00347
31. Alavi S.M.N., Arvin M.J., Kalantari K.M. 2014. Salicylic acid and nitric oxide alleviate osmotic stress in wheat (Triticum aestivum L.) seedlings. J. Plant Interact. 9 (1) : 683-688.
32. Alscher R.G., Erturk N., Heath L.S. 2002. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J. Exp. Bot. 53 : 1331-1341.
33. Antoniou C., Savvides A., Christou A., Fotopoulos V. 2016. Unravelling chemical priming machinery in plants: the role of reactive oxygen-nitrogen-sulfur species in abiotic stress tolerance enhancement. Curr. Opin. Plant Biol. 33 : 101-107.
34. Arasimowicz-Jelonek M., Floryszak-Wieczorek J., Gwóźdź E.A. 2011. The message of nitric oxide in cadmium challenged plants. Plant Sci. 181 (5) : 612-620.
35. Arasimowicz-Jelonek M., Floryszak-Wieczorek J., Deckert J., Rucińska-Sobkowiak R., Gzyl J., Pawlak-Sprada S., Abramowski D., Jelonek T., Gwóźdź E.A. 2012. Nitric oxide implication in cadmium-induced programmed cell death in roots and signaling response of yellow lupine plants. Plant Physiol. Biochem. 58. : 124-134.
36. Arora D., Bhatla S.C. 2015. Nitric oxide triggers a concentration-dependent differential modulation of superoxide dismutase (FeSOD and Cu/ZnSOD) activity in sunflower seedling roots and cotyledons as an early and long. Plant Signal. Behav. 10 (10) : e1071753. - doi: 10.1080/15592324.2015.1071753
37. Arora D., Jain P., Singh N., Kaur H., Bhatla S.C. 2016. Mechanisms of nitric oxide crosstalk with reactive oxygen species scavenging enzymes during abiotic stress tolerance in plants. Free Radical Res. 50 : 291-303. doi: 10.3109/10715762.2015. 1118473
38. Astier J., Lindermayr C. 2012. Nitric oxide-dependent posttranslational modification in plants: an update. Int. J. Mol. Sci. 13 : 15193-15208.
39. Bai X, Yang L, Tian M, Chen J, Shi J, Yang Y, Hu X. 2011. Nitric oxide enhances desiccation tolerance of recalcitrant Antiaris toxicaria seeds via protein Snitrosylation and carbonylation. PLoS One. e20714.
40. Barand A., Nasibi F., ManouchehriKalantari Kh. 2015. The effect of arginine pretreatment in the increase of coldtolerance in Pistacia vera L. in vitro. Russ. Agricult. Sci. 41 (5) : 340-346.
41. Bartoli C.G., Casalongueb C.A., Simontacchia M. Marquez-Garciac B., Foyer C.H. 2013. Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environ. Exp. Bot. 94 : 73-88.
42. Baudouin E., Hancock J.T. 2013. Nitric oxide signaling in plants. Front. Plant Sci. 4 : 553. doi: 10.3389/fpls.2013.00553
43. Baxter A., Mittler R., Suzuki N. 2014. ROS as key players in plant stress signalling. J. Exp. Bot. 65 : 1229-1240.
44. Beltran B., Orsi A., Clementi E., Moncada S. 2000. Oxidative stress and S-nitrosylation of proteins in cells. Br. J. Pharmacol. 129 : 953-960.
45. Brown G.C. 1995. Nitric oxide regulates mitochondrial respiration and cell functions by inhibiting cytochrome oxidase. FEBS Lett. 369 : 136-139.
46. Brunelli L., Yermilov V., Beckman J.S. 2001. Modulation of catalase peroxidatic and catalatic activity by nitric oxide. Free Radical Bio Med. 30 : 709-714.
47. Capone R., Tiwari B.S., Levine A. 2004. Rapid transmission of oxidative and nitrosative stress signals from roots to shoots in Arabidopsis. Plant Physiol. Biochem. 42 : 425-428.
48. Chaki M., Valderrama R., Fernández-Ocaña A.M., Carreras A., Gómez-Rodríguez M.V., Pedrajas J.R., Begara-Morales J.C., Sánchez-Calvo B., Luque F., Leterrier M., Corpas F.J., Barroso J.B. 2011. Mechanical wounding induces a nitrosative stress by downregulation of GSNO reductase and a rise of Snitrosothiols in sunflower (Helianthus annuus) seedlings.J. Exp. Bot. 62 : 1803-1813.
49. Chakraborty N., Acharya K. 2017. "NO way"! Says the plant to abiotic stress. Plant Gene. doi: 10.1016/j.plgene.2017.05.001
50. Clark D., Dunar J., Navarre D.A., Klessig D.F. 2000. Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant-Microbe Interact. 14 : 1380-1384.
51. Clarke A., Desikan R., Hurst R.D., Hancock J.T., Neill S.J. 2000. NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant J. 24 : 667-677.
52. Cooper C.E. 1999. Nitric oxide and iron proteins. Biochem Biophys Acta. 1411 : 290-309.
53. Corpas F.J., Barroso J.B. 2017. Nitric oxide synthase-like activity in higher plants. Nitric Oxide. doi: 10.1016/j.niox.2016.10.009
54. Correa-Aragunde N., Graziano M., Lamattina L. 2004. Nitric oxide plays a central role in determining lateral root development in tomato. Planta. 218 : 900-917.
55. Courtois C., Besson A., Dehan J., Bourque S., Dobrowolska G., Pugin A., Wendehenne D. 2008. Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases. J. Exp. Bot. 59 : 155-163.
56. Crawford N.M. 2005. Mechanisms for nitric oxide synthesis in plants. J. Exp. Bot. 57 : 471-478.
57. Crawford N.M., Guo F.Q. 2005.New insights into nitric oxide metabolism and regulatory functions. Trends Plant Sci. 10 : 195-200.
58. Cui J.X., Zhou Y.H., Ding J.G., Xia X.J., Shi K., Chen S.C., Asami T., Chen Z., Yu J.Q. 2011. Role of nitric oxide in hydrogen peroxide-dependent induction of abiotic stress tolerance by brassinosteroids in cucumberpce. Plant Cell Environ. 34 : 347-358.
59. de Montaigu A., Sanz-Luque E., Galvan A., Fernandez E. 2010. A soluble guanylate cyclase mediates negative signalling by ammonium on expression of nitrate reductase in Chlamydomonas. Plant Cell. 22 : 1532-1548.
60. del Giudice J., Cam Y., Damiani I., Fung-Chat F., Meilhoc E., Bruand C., Brouquisse R., Puppo A., Boscari A. 2011. Nitric oxide is required for an optimal establishment of the Medicago truncatula - Sinorhizobium meliloti symbiosis. New Phytol. 191 : 405-417.
61. del Rio L.A., Sandalio L.M., Corpas F.J., Palma J.M., Barroso J.B. 2006. Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol. 141 : 330-335.
62. Delledonne M., Xia Y., Dixon R.A., Lamb C. 1998.Nitric oxide functions as a signal in plant disease resistance.Nature. 394 : 585-588.
63. Deng X.G., Zhu T., Zou L.J., Han X.Y., Zhou X., Xi D.H., Zhang D.W., Lin H.H. 2016. Orchestration of hydrogen peroxide and nitric oxide in brassinosteroid-mediated systemic virus resistance in Nicotiana benthamiana. Plant J. 85 : 478-493.
64. Diniz M.C., Olivon V.C., Tavares L.D., Simplicio J.A., Gonzaga N.A., de Souza D.G., Bendhack L.M., Tirapelli C.R., Bonaventura D. 2017.Mechanisms underlying sodium nitroprusside-induced tolerance in the mouse aorta: role of ROS and cyclooxygenase-derived prostanoids. Life Sci. 176 : 26-34.
65. Durner J., Wendehemme D., Klessig D.F. 1998. Defense gene induction in tobacco by nitric oxide, cyclic GMP and cyclic ADP-ribose. Proc Natl. Acad. Sci. USA. 95 : 10328-10333.
66. El-beltagi H.S., Ahmed O.K., Hegazy A.E. 2016. Protective effect of nitric oxide on high temperature induced oxidative stress in wheat (Triticum aestivum) callus culture. Not. Sci. Biol. 8 (2) : 192-198.
67. Fancy N.N., Bahlmann A.K., Loake G.J. 2017. Nitric oxide function in plant abiotic stress. Plant Cell Environ. 40 (4) : 462-472.
68. Farnese F.S., Menezes-Silva P.E., Gusman G.S., Oliveira J.A. 2016. When bad guys become good ones: the key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress.Front. Plant Sci. 7 : 471.
69. Ford P.C. 2010. Reactions of NO and nitrite with heme models and proteins. Inorg. Chem. 49 : 6226-6239.
70. Foyer C.H., Noctor G. 2009. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid. Redox Signal. 11 : 861-906.
71. Freschi L. 2013. Nitric oxide and phytohormone interactions: current status and perspectives. Front. Plant Sci. 4 : 398.
72. Gémes K., Poór P., Horváth E., Kolbert Z., Szopkó D., Szepesi A., Tari I. 2011. Cross-talk between salicylic acid and NaCl-generated reactive oxygen species and nitric oxide in tomato during acclimation to high salinity. Physiol. Plant. 142 : 179-192.
73. Gonzalez A., Cabrera A.M., Henriquez M.J., Contreras R.A., Morales B., Moenne A. 2012. Cross talk among calcium, hydrogen peroxide, and nitric oxide and activation of gene expression involving calmodulins and calcium-dependent protein kinases in Ulva compressa exposed to copper excess. Plant Physiol. 158 : 1451-1462.
74. Gould K.S., Lamotte O., Klinguer A., Pugin A., Wendehenne D. 2003. Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ. 26 : 1851-1862.
75. Gupta K.J., Kaiser W.M. 2010. Production and scavenging of nitric oxide by barley root mitochondria. Plant Cell Physiol. 51 : 576-584.
76. He J.M., Ma X.G., Zhang Y., Sun T.F., Xu F.F., Chen Y.P., Liu X., Yue M. 2013. Role and interrelationship of Gα protein, hydrogen peroxide, and nitric oxide in ultraviolet B-induced stomatal closure in Arabidopsis leaves. Plant Physiol. 161 : 1570-1583.
77. Hsu Y.T., Kao C.H. 2004. Cadmium toxicity is reduced by nitric oxide in rice leaves.Plant Growth Regul. 42 : 227-238.
78. Hsu Y.Y., Kao C.H. 2011. Nitric oxide is involved in methyl jasmonate induced lateral root formation in rice. Crop Environ. Bioinformatics. 8 : 160-167.
79. Huang X., Stettmaier K., Michel C., Hutzler P., Mueller M.J., Durner J. 2004. Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta. 218 : 938-946.
80. Ischiropoulos H. 2003. Biological selectivity and functional aspects of protein tyrosine nitration. Biochem. Biophys. Res. Commun. 305 : 776-783.
81. Karpets Yu.V., Kolupaev Yu.E., Yastreb T.O. 2015. Signal mediators at induction of heat resistance of wheat plantlets by short-term heating. Ukr. Biochem. J. 87 (6) : 104-112.
82. Khan M.N., Mohammad F., Mobin M., Ali Saqib M. 2014.Tolerance of plants to abiotic stress: a role of nitric oxide and calcium. In: Nitric Oxide in Plants: Metabolism and Role in Stress Physiology (Eds. Khan M.N. et al.). Springer International Publishing Switzerland, doi: 10.1007/978-3-319-06710-0_14.
83. Klepper L. 1991. NOx evolution by soybean leaves treated with salicylic acid and selected derivatives. Pest. Biochem. Physiol. 39 : 43-48.
84. Klessig D.F., Durner J., Noad R., Navarre D.A., Wendehenne D., Kumar D., Zhou J.M., Shah J., Zhang S., Kachroo P., Trifa Y., Pontier D., Lam E., Silva H. 2000. Nitric oxide and salicylic acid signalling in plant defense. Proc. Natl. Acad. Sci. 97 : 8849-8855.
85. Kolupaev Yu.E., Karpets Yu.V., Dmitriev A.P. 2015. Signal mediators in plants in response to abiotic stress: calcium, reactive oxygen and nitrogen species. Cytol. Genet. 49 (5) : 338-348.
86. Krasylenko Y.A., Yemets A.I., Sheremet Y.A., Blume Ya.B. 2012.Nitric oxide as a critical factor for perception of UV-B irradiation by microtubules in Arabidopsis. Physiol. Plant. 145 : 505-515.
87. Lamotte O., Courtois C., Barnavon L., Pugin A.,Wendehenne D. 2005. Nitric oxide in plants: the biosynthesis and cell signaling properties of a fascinating molecule. Planta. 221 : 1-4.
88. Lamotte O., Guold K., Lecourieux D., Sequeira-Legrand A., Lebrun-Garcia A., Durner J., Pugin A., Wendehenne D. 2004.Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol. 135 : 516-529.
89. Lamotte O.C., Courtois G., Dobrowolska A. Besson A., Pugin A., Wendehenne D. 2006. Mechanism of nitric-oxide-induced increase of free cytosolic Ca2+ concentration in Nicotiana plumbaginifolia cells. Free Radic. Biol. Med. 40 : 1369-1376.
90. Lanteri M., Pagnussat G.C., Lamattina L. 2006. Calcium and calcium-dependent protein kinases are involved in nitric oxide and auxin-induced adventitious root formation in cucumber. J. Exp. Bot. 57 : 1341-1351.
91. Lanteri M.L., Laxalt A.M., Lamattina L. 2008. Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in Cucumber. Plant Physiol. 147 : 188-198.
92. Laspina N.V., Groppa M.D., Tomaro M.L., Benavides M.P. 2005. Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci. 169 : 323-330.
93. Laxalt A.M., Raho N., Ten Have A., Lamattina L. 2007.Nitric oxide is critical for inducing phosphatidic acid accumulation in xylanase-elicited tomato cells. J. Biol. Chem. 282 : 21160-21168.
94. Lecourieux D., Mazars C., Pauly N., Ranjeva R., Pugin A. Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell. - 2002. 14 2627-2641.
95. Li Z.G., Yang S.Z., Long W.B., Yang G.X., Shen Z.Z. 2013. Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ. 36 : 1564-1572.
96. Liu S., Dong Y., Xu L., Kong J. 2014. Effects of foliar applications of nitric oxide and salicylic acid on salt-induced changes in photosynthesis and antioxidative metabolism of cotton seedlings. Plant Growth Regul. 73 : 67-78.
97. Lozano-Juste J., Colom-Moreno R., Leon J. 2011. In vivo protein tyrosine nitration in Arabidopsis thaliana. J. Exp. Bot. 62 : 3501-3517.
98. Ludidi N., Gehring C. 2003. Identification of a novel protein with guanylyl cyclase activity in Arabidopsis thaliana. J. Biol. Chem. 278 : 6490-6494.
99. Malyshev I.Yu., Manukhina E.B., Mikoyan V.D., Kubrina L.N., Vanin A.F. 1995. Nitric oxide is involved in heat-induced HSP70 accumulation. FEBS Lett. 370 (3) : 159-162.
100. Marino D., Dunand C., Puppo A., Pauly N. 2012. A burst of plant NADPH oxidases. Trends Plant Sci. 17 : 9-15.
101. Minibayeva F., Beckett R.P. 2015. The roles of plant peroxidases in the metabolism of reactive nitrogen species and other nitrogenous compounds. In: Reactive Oxygen and Nitrogen Species Signaling and Communication in Plants (Eds. Gupta K.J., Igamberdiev A.U.). Signaling and Communication in Plants. 23. Switzerland : Springer International Publishing : 43-62
102. Minibayeva F.V., Gordon L.K., Kolesnikov O.P., Chasov A.V. 2001. Role of extracellular peroxidase in the superoxide production by wheat root cells. Protoplasma. 217 (1-3) : 125-128.
103. Mur L.A.J., Santosa I.E., Laarhoven L.J., Harren J.F., Smith A.R. 2003. A new partner in the danse Macabre: The role of nitric oxide in the hypersensitive response. Bulg. J. Plant Physiol. Spec. Issue : 110-123.
104. Mur L.A.J., Mandon J., Persijn S., Cristescu S.M., Moshkov I.E., Novikova G.V., Hall M.A., Harren F.J.M., Hebelstrup K.H., Gupta K.J. 2013. Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants. 5: pls052. doi 10.1093/aobpla/pls052
105. Mur L.A.J., Prats E., Pierre S., Hall M.A., Hebelstrup K.H. 2013. Integrating nitric oxide into salicylic acid and jasmonic acid/ethylene plant defense pathways. Front. Plant Sci. 4 : 215.
106. Neill S.J., Desikan R., Clarke A., Hurst R.D., Hancock J.T. 2002. Hydrogen peroxide and nitric oxide as signalling molecules in plants. J. Exp. Bot. 53 : 1237-1247.
107. Neill S., Bright J., Desikan R., Hancock J., Harrison J., Wilson I. 2008. Nitric oxide evolution and perception. J. Exp. Bot. 59 : 25-35.
108. Nilanjan C., Krishnendu A. 2017. "NO way"! Says the plant to abiotic stress. Plant Gene. doi: 10.1016/j.plgene.2017.05.001
109. Niu L., Liao W. 2016. Hydrogen peroxide signalingin plant development and abiotic responses: Crosstalk with nitric oxide and calcium. Front. Plant Sci. 7 : 230.
110. Ogasawara Y., Kaya H., Hiraoka G., Yumoto F., Kimura S., Kadota Y., Hishinuma H., Senzaki E., Yamagoe S., Nagata K., Nara M., Suzuki K., Tanokura M., Kuchitsu K. 2008. Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J. Biol. Chem. 283 : 8885-8892.
111. Oz M.T., Eyidogan F., Yucel M., Oktem H.A. 2015. Functional role of nitric oxide under abiotic stress conditions. In: Nitric Oxide Action in Abiotic Stress Responses in Plants (Eds. Khan M.N., Mobin M., Mohammad F., Corpas F.J.) Heidelberg, New York, Dordrecht, London : 21-42.
112. Radi R. 2004.Nitric oxide, oxidants, and protein tyrosine nitration. Proc. Natl. Acad. Sci. USA. 101 : 4003-4008.
113. Rosales E.P., Iannone M.F., Groppa M.D., Benavides M.P. 2011.Nitric oxide inhibits nitrate reductase activity in wheat leaves. Plant Physiol. Biochem. 49 : 124-130.
114. Roszer T. 2014. Biosynthesis of nitric oxide in plants. In: Nitric Oxide in Plants: Metabolism and Role in Stress Physiology (Eds. Khan M.N. et al.). Springer International Publishing Switzerland : 17-32. doi: 10.1007/978-3-319-06710-0_2
115. Savvides A., Ali S., Tester M., Fotopoulos V. 2016. Chemical priming of plants against multiple abiotic stresses: mission possible?. Trends Plant Sci. 21 : 329-340.
116. Seabra A.B., Oliveira H.C. 2016. How nitric oxide donors can protect plants in a changing environment: what we know so far and perspectives. AIMS Mol. Sci. 3 (4) : 692-718.
117. Shan C., Zhou Y., Liu M. 2015. Nitric oxide participates in the regulation of the ascorbate-glutathione cycle by exogenous jasmonic acid in the leaves of wheat seedlings under drought stress. Protoplasma. 252 : 1397-1405.
118. Shi F.-M., Li Y.-Z. 2008. Verticillium dahliae toxins-induced nitric oxide production in Arabidopsis is major dependent on nitrate reductase. BMB Rep. 41 : 79-85.
119. Siddiqui M.H., Alamri S.A., Al-Khaishany M.Y.Y., Al-Qutami M.A., Ali H.M., Khan M.N. 2017. Nitric oxide and calcium induced physiobiochemical changes in tomato (Solanum lycopersicum) plant under heat stress. Fresenius Environ. Bull. 26 (2a) : 1663-1672.
120. Siddiqui M.H., Al-Whaibi M.H., Ali H.M., Sakran A.M., Basalah M.O., AlKhaishany M.Y.Y. 2013. Mitigation of nickel stress by the exogenous application of salicylic acid and nitric oxide in wheat. Australian J. Crop Sci. 7 : 1780-1788.
121. Singh H.P., Batish D.R., Kaur G., Arora K., Kohli R.H. 2008. Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ. Exp. Bot. 63 : 158-167.
122. Singh R.J., Hogg N., Goss S.P.A., Antholine W.E., Kalyanaraman B. 1999. Mechanism of superoxide dismutase/H2O2-mediated nitric oxide release from Snitrosoglutathione-role of glutamate. Arch. Biochem. Biophys. 372 : 8-15.
123. Sokolovski S., Hills A., Gay R., Garcia-Mata C., Lamattina L., Blatt M.R. 2005. Protein phosphorylation is a prerequisite for intracellular Ca2+ release and ion channel control by nitric oxide and abscisic acid in guard cells. Plant J. 43 : 520-529.
124. Song L., Ding W., Zhao M., Sun B., Zhang L. 2006. Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Sci. 171 : 449-458.
125. Straltsova D., Chykun P., Subramaniam S., Sosan A., Kolbanov D., Sokolik A., Demidchik V. 2015. Cation channels are involved in brassinosteroid signalling in higher plants. Steroids. -97 98-106.
126. Tewari R.K., Hahn E.J., Paek K.Y. 2008. Function of nitric oxide and superoxide anion in the adventitious root development and antioxidant defence in Panax ginseng. Plant Cell Rep. 27 : 563-573.
127. Tewari R.K., Paek K.Y. 2011. Salicylic acid-induced nitric oxide and ROS generation stimulate ginsenoside accumulation in Panax ginseng roots. J Plant Growth Regul. 30 : 396-404.
128. Thapa G., Sadhukhan A., Panda S.K., Sahoo L. 2012. Molecular mechanistic model of plant heavy metal tolerance. Biometals. 25 : 489-505.
129. Tuteja N., Sopory S.K. 2008. Chemical signaling under abiotic stress environment in plants. Plant Signal. Behav. 3 : 525-536.
130. Uchida A., Jagendorf A.T., Hibino T., Takabe T., Takabe T. 2002. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci. 163 : 515-523.
131. Wang P.G., Xian M., Tang X., Wu X., Wen Z., Cai T., Janczuk A.J. 2002. Nitric oxide donors: chemical activities and biological applications. Chem. Rev. 102 : 1091-1134.
132. Wang Y., Loake G.J., Chu C. 2013. Cross-talk of nitric oxide and reactive oxygen species in plant programed cell death. Front. Plant Sci. 4 : 314. doi:10.3389/fpls.2013.00314
133. Wang Y., Li L., Cui W., Xu S., Shen W., Wang R. 2012. Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil. 351 : 107-119.
134. Wang W.H., Yi X. Q., Han A.D., Liu T.W., Chen J., Wu F.H., Dong X.J., He J.X., Pei Z.M., Zheng H.L. 2012. Calcium-sensing receptor regulates stomatal closure through hydrogen peroxide and nitric oxide in response to extracellular calcium in Arabidopsis. J. Exp. Bot. 63 : 177-190.
135. Wilson I.D., Neill S.J., Hancock J.T. 2008. Nitric oxide synthesis and signaling in plants. Plant Cell Environ. 31 : 622-631.
136. Wimalasekera R., Villar C., Begum T., Scherer G.F. 2001. Coper amine oxidase1 (CuAO) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction. Mol. Plant. 4 : 663-678.
137. Wink D.A., Hanbauer I., Krishna M.C., DeGraff W., Gamson J., Mitchell J.B. 1993. Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc. Natl. Acad. Sci. USA. 90 : 9813-9817.
138. Wong H.L., Pinontoan R., Hayashi K., Tabata R., Yaeno T., Hasegawa K., Kojima C., Yoshioka H., Iba K., Kawasaki T., Shimamoto K. 2007. Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell. 19 : 4022-4034.
139. Xing H., Tan L., An L., Zhao Z., Wang S., Zhang C. 2004. Evidence for the involvement of nitric ox-ide and reactive oxygen species in osmotic stress tolerance of wheat seed-lings: inverse correlation between leaf abscisic acid accumulation and leaf water loss. Plant Growth Regul. 42 : 61-68.
140. Xu M.J., Dong J.F., Zhang X.B. 2008. 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. 51 : 676-686.
141. Xu M.J., Dong J.F., Zhang X.B. 2008.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. 51 : 676-686.
142. Xu J., Yin H., Li Y., Liu X. 2010. Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum. Plant Physiol. 154 : 1319-1334.
143. Xu Yu., Sun X. , Jin J., Zhou H. 2010. Protective effect of nitric oxide on light-induced oxidative damage in leaves of tall fescue. J. Plant Physiol. 167 : 512-518.
144. Yan J., Guan L., Sun Y., Zhu Y., Liu L., Lu R., Jiang M., Tan M., Zhang A. 2015. Calcium and ZmCCaMK are involved in brassinosteroid-induced antioxidant defense in maize leaves. Plant Cell Physiol. 56 : 883-896.
145. Yun B.W., Feechan A., Yin M., Saidi N.B.B., Le Bihan T., Yu M., Moore J.W., Kang J.G., Kwon E., Kang J.G., Spoel S.H., Pallas J.A., Loake G.J. 2011. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature. 478 : 264-268.
146. Zhang A., Zhang J., Zhang J., Ye N., Zhang H., Tan M., Jiang M. 2011. Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. Plant Cell Physiol. 52 : 181-192.
147. Zhang Y., Wang L., Liu Y., Zhang Q., Wei Q., Zhang W. 2006.Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta. 224 : 545-555.
148. Zhang A., Jiang M., Zhang J. Ding H., Xu S., Hu X., Tan M. 2007. Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytol. 175 : 36-50.
149. Zhao Y., Qi Z., Berkowitz G.A. Teaching an old hormone new tricks: cytosolic Ca2+ elevation involvement in plant brassinosteroid signal transduction cascades. Plant Physiol. 2013. 163 : 555-565.
150. Zhou S., Jia L., Chu H., Wu D., Peng X., Liu X., Zhang J., Zhao J., Chen K., Zhao L. 2016. Arabidopsis CaM1 and CaM4 promote nitric oxide production and salt resistance by inhibiting S-nitrosoglutathione reductase via direct binding. PLOS Genet. 12 (9) : e1006255. doi:10.1371/journal. pgen.1006255
151. Zhu T., Deng X.G., Tan W.R., Zhou X., Luo S.S., Han X.Y., Zhang D.W., Lin H.H. 2016. Nitric oxide is involved in brassinosteroid-induced alternative respiratory pathway in Nicotiana benthamiana seedlings' response to salt stress. Physiol. Plant. 156 : 150-163.