Visn. Hark. nac. agrar. univ., Ser. Biol., 2019, Issue 2 (47), pp. 39-60


https://doi.org/10.35550/vbio2019.02.039




ANTIOXIDANT PROTECTION IN PLANTS UNDER HEAT STRESS


Yu. E. Kolupaev1, 2, T. O. Yastreb1, O. I. Kokorev1

1Dokuchaev Kharkiv National Agrarian University
(Kharkiv, Ukraine)
E-mail:
plant_biology@ukr.net
2Karazin Kharkiv National University
(Kharkiv, Ukraine)


Antioxidant system is one of the non-specific components of plant resistance. The review examines its role in plant resistance to hyperthermia. One of the effects of high temperature on plants is raising membrane fluidity, which increases the probability of formation of reactive oxygen species (ROS) in the electron transport chain of chloroplasts and mitochondria. Under the action of high temperatures on plants, NADPH oxidase, a key enzyme generating the superoxide anion radical, is also activated. A moderate increase in the generation of ROS along with activation of the signal network as a whole and a transient increase in the concentration of cytosolic calcium, the intracellular content of nitric oxide (NO) acts as a mechanism inducing the formation of an adaptive response – an increase in antioxidant activity. The review describes the effects of changes in gene expression and the activity of key antioxidant enzymes in plants of different species in response to hyperthermia. Special attention is paid to the role of superoxide dismutase, which can be involved not only in antioxidant protection, but also in the formation of the signal pool of hydrogen peroxide. The role in hyperthermia resistance of other components of the antioxidant defense system, in particular, glutathione, proline, sugars and polyunsaturated fatty acids of membranes, which are recently considered as supramolecular antioxidants, is also analyzed. Characterized by methods of inducing the antioxidant system of plants and their resistance to hyperthermia using exogenous exposure signaling agents – hydrogen peroxide, donors of NO and H2S, as well as individual phytohormones (salicylic acid and brassinosteroids). It is noted that the effects of inducing the antioxidant system, in many cases, can increase the resistance of plants not only to hyperthermia, but also to other stress factors, that is, cause a manifestation of cross-tolerance.


Key words: hyperthermia, antioxidant system, reactive oxygen species, redox homeostasis, biomembranes, signal mediators, cross-tolerance

 


REFERENCES


1. Abramchik L.M., Serdiuchenko E.V., Makarov V.N., Zenevich L.A., Zavoronkova N.B., Kabaschnikova L.F. 2014.Variety specific features of plant response of spring hexploid triticale to the heat shock. Proc. Natl. Acad. Sci Belarus. Biol. Ser. 4 : 43-49. (In Russian)
 
2. Al'terhot V.F. 1981. Effect of high temperature on the plant in experiment and nature. Moscow : 57 p. (In Russian)
 
3. Kabaschnikova L.F., Abramchik L.M., Serdiuchenko E.V., Kapylova L.V. 2013. Response of barley seedling (Hordeum vulgare) to the combination actions of hyperthermia and dehydration. Proc. Natl. Acad. Sci Belarus. Biol. Ser. 3 : 60-66. (In Russian)
 
4. Karpets Yu.V. Role of calcium ions and reactive oxygen species in induction of antioxidant enzymes and heat resistance of plant cells by nitric oxide donor. Visn. Hark. nac. agrar. univ., Ser. Biol. (Bull. Kharkiv Natl. Agrar. Univ. Ser. Biology). 3 (42) : 52-61. (In Russian)
 
5. Karpets Yu.V., Kolupaev Yu.E. 2018. Participation of nitric oxide in 24-epibrassinolide-induced heat resistance of wheat coleoptiles: functional interactions of nitric oxide with reactive oxygen species and Ca ions. Russ. J. Plant Physiol. 65 (2) : 177-185.
https://doi.org/10.1134/S1021443718010053
 
6. 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.
https://doi.org/10.1134/S1021443714060090
 
7. 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) : 1027-1033.
https://doi.org/10.1134/S1021443711060094
 
8. Karpets Y.V., Kolupaev Y.E., Yastreb T.O., Oboznyi A.I. 2015b. Effects of NO-status modification, heat hardening, and hydrogen peroxide on the activity of antioxidant enzymes in wheat seedlings. Russ. J. Plant Physiol.. 62 (3) : 292-298.
https://doi.org/10.1134/S1021443715030097
 
9. Karpets Yu.V., Kolupaev Yu.E., Yastreb T.O., Oboznyi A.I. 2016. Induction of heat resistance of wheat plantlets by exogenous calcium, hydrogen peroxide and donor of nitric oxide: functional interaction of signal mediators. Russ. J. Plant Physiol. 63 (4) : 490-498.
https://doi.org/10.1134/S1021443716040075
 
10. Kolupaev, Yu.E., 2016. Plant cell antioxidants and their role in ROS signaling and plants resistance. Usp. Sovrem. Biol. 136 : 181-198.
 
11. Kolupaev Yu.E., Vayner A.A., Yastreb T.O., Oboznyi A.I., Khripach V.A. 2014. 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. 50 (6) : 658-663. Doi: 10.1134/S0003683814060076
https://doi.org/10.1134/S0003683814060076
 
12. Kolupaev Yu.Ye., Karpets Yu.V. 2008. Oxidative stress and the state of antioxidative system in wheat coleoptiles at the action of hydrogen peroxide and heating. Visn. Hark. nac. agrar. univ., Ser. Biol. (Bull. Kharkiv Natl. Agrar. Univ. Ser. Biology). 2 (14) : 42-52. (In Russian)
 
13. Kolupaev Yu.E., Karpets Yu.V. 2017. Role of signal mediators and stress hormones in regulation of plants antioxidative system. Fisiol. rast. genet. 49 (6) : 463-481. (In Russian)
https://doi.org/10.15407/frg2017.06.463
 
14. Kolupaev Yu.E., Karpets Yu.V., Yastreb T.O., Lugovaya A.A. Signal mediators in realization of physiological effects of stress phytohormones. Visn. Hark. nac. agrar. univ., Ser. Biol. (Bull. Kharkiv Natl. Agrar. Univ. Ser. Biology). 1 (37) : 42-62. (In Russian)
 
15. Kolupaev Yu.E., Oboznyi O.I. Participation of the active oxygen forms in the induction of ascorbate peroxidase and guaiacol peroxidase under heat hardening of wheat seedlings. Ukr Biokhim Zhurn. 2012. 84 (6) : 131-138. (In Russian)
 
16. Kolupaev Yu.E., Oboznyi A.I., Shvidenko N.V. 2013. Role of hydrogen peroxide in generation of a signal inducing heat tolerance of wheat seedlings. Russ. J. Plant Physiol. 60 (2) : 227-234. Doi: 10.1134/S102144371302012X
https://doi.org/10.1134/S102144371302012X
 
17. Kolupaev Yu.E., Fіrsova E.N., Yastreb T.O., Lugovaya A.A. 2017. The participation of calcium ions and reactive oxygen species in the induction of antioxidant enzymes and heat resistance in plant cells by hydrogen sulfide donor. Appl. Biochem. Microbiol. 53 (5) : 573-579. Doi: 10.1134/S0003683817050088
https://doi.org/10.1134/S0003683817050088
 
18. 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. Doi: 10.1134/S0003683812050055
https://doi.org/10.1134/S0003683812050055
 
19. Kosakovskaya I.V. 2008. Plant Stress Proteins. Kiev : 150 p. (In Russian)
 
20. Kreslavski V.D., Carpentier R., Klimov V.V., Murata N., Allakhverdiev S.I. Molecular Mechanisms of Stress Resistance of Photosynthetic Apparatus. Biol. Membrany. 24 (3) : 195-217. (In Russian)
 
21. Kreslavski V.D., Zorina A.A. Los' D.A., Allakhverdiev S.I. Molecular mechanisms of adaptation of the photosynthetic apparatus to stress. In: Modern Problems of Photosynthesis. V. 2. Izhevsk : 544 p. (In Russian)
 
22. Los' D.A. Cyanobacterial Sensory Systems. Moscow : 218 p. (In Russian)
 
23. Martinovich G.G., Cherenkevich S.N. Redox Processes in Cells. Minsk : 159 p. (In Russian)
 
24. Nilova I.A. 2019. Resistance of Wheat Plants to High-Temperature Action of Varying Intensity: Physiological, Biochemical and Molecular Genetic Aspects. PhD Diss. (Biol.). Petrozavodsk: 163 p. (In Russian)
 
25. Nilova I.A., Topchieva L.V., Titov A.F. 2015. HSP gene expression in wheat under heat stress. Trudy KarNC RAN. Ser. Eksperiment. Biologiya. 11 : 55-65. Doi: 10.17076/eb240 (In Russian)
https://doi.org/10.17076/eb240
 
26. Radyukina N.L., Toaima V.I.M., Zaripova N.R. 2012. The involvement of low-molecular antioxidants in cross-adaptation of medicine plants to successive action of UV-B radiation and salinity. Russ. J. Plant Physiol. 59 (1) : 71-78.
https://doi.org/10.1134/S1021443712010165
 
27. Titov A.F., Talanova V.V. Plant Resistance and Phytohormones. Petrozavodsk: 206 p. (In Russian)
 
28. Agrawal D., Allakhverdiev S.I., Jajoo A. 2016. Cyclic electron flow plays an important role in protection of spinach leaves under high temperature stress. Russ. J. Plant Physiol. 63 (2) : 210-215. Doi: org/10.1134/S1021443716020023
https://doi.org/10.1134/S1021443716020023
 
29. Akter N., Islam M.R. 2017. Heat stress effects and management in wheat. A review. Agron. Sustain. Dev. 37 : 37. Doi 10.1007/s13593-017-0443-9
https://doi.org/10.1007/s13593-017-0443-9
 
30. Allakhverdiev S., Kreslavski V., Klimov V., Los D., Carpentier R., Mohanty P. 2008. Heat stress: An overview of molecular responses in photosynthesis. Photosynth. Res. 98 : 541-550. Doi: 10.1007/s11120-008-9331-0
https://doi.org/10.1007/s11120-008-9331-0
 
31. Almeselmani M., Deshmukh P.S., Sairam R.K., Kushwaha S.R., Singh T.P. 2006. Protective role of antioxidant enzymes under high temperature stress. Plant Sci. 171 : 382-388. Doi: 10.1016/j.plantsci.2006.04.009
https://doi.org/10.1016/j.plantsci.2006.04.009
 
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.
https://doi.org/10.1093/jxb/53.372.1331
 
33. 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
https://doi.org/10.3109/10715762.2015.1118473
 
34. Asthir B. 2015. Mechanisms of heat tolerance in crop plants. Biol Plant. 59 (4) : 620-628. Doi: org/10.1007/s10535-015-0539-5
https://doi.org/10.1007/s10535-015-0539-5
 
35. Astier J., Lindermayr C. 2012. Nitric oxide-dependent posttranslational modification in plants: an update. Int. J. Mol. Sci. 13 : 15193-15208. Doi: 10.3390/ijms131115193
https://doi.org/10.3390/ijms131115193
 
36. Bita C.E., Gerats T. 2013. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front. Plant Sci. 4 : 273. doi: 10.3389/fpls.2013.00273
https://doi.org/10.3389/fpls.2013.00273
 
37. Bernfur K., Rutsdottir G., Emanuelsson C. 2017. The chloroplast-localized small heat shock protein Hsp21 associates with the thylakoid membranes in heat-stressed plants. Protein Sci. 26 : 1773-1784. Doi: 10.1002/pro.3213
https://doi.org/10.1002/pro.3213
 
38. Camejo D., Jiménez A., Alarcón J.J., Torres W., Gómez J.M., Sevilla F. 2006. Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants. Funct. Plant Biol. 33 : 177-187. Doi: org/10.1071/FP05067
https://doi.org/10.1071/FP05067
 
39. Cheng T., Shi J., Dong Y., Ma Y., Peng Y., Hu X., Chen J. 2018. Hydrogen sulfide enhances poplar tolerance to high-temperature stress by increasing S-nitrosoglutathione reductase (GSNOR) activity and reducing reactive oxygen/nitrogen damage. Plant Growth Regul. 84 : 11-23. doi: org/10.1007/s10725-017-0316-x
https://doi.org/10.1007/s10725-017-0316-x
 
40. Choudhury F.K., Rivero R.M., Blumwald E., Mittler R. 2017. Reactive oxygen species, abiotic stress and stress combination. Plant J. 90 : 856-867. Doi: 10.1111/tpj.13299
https://doi.org/10.1111/tpj.13299
 
41. Christou A., Filippou P., Manganaris G. A., Fotopoulos V. 2014. Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin. BMC Plant Biol. 14 : 42. Doi: 10.1186/1471-2229-14-42
https://doi.org/10.1186/1471-2229-14-42
 
42. Cooper C.E. 1999. Nitric oxide and iron proteins. Biochem. Biophys. Acta. 1411 : 290-309.
https://doi.org/10.1016/S0005-2728(99)00021-3
 
43. Cuevasanata E., Lange M., Bonanata J., Coitino E.L., Ferrer-Sueta G., Filipovic M.R., Alvarez B. 2015. Reaction of hydrogen sulphide with disulfide and sulfenic acid to form the strongly nucleophilic persulfide. J. Biol. Chem. 290 (45) : 26866-26880. Doi: 10.1074/jbc.M115.672816
https://doi.org/10.1074/jbc.M115.672816
 
44. Dash S., Mohanty N. 2002. Response of seedlings to heat-stress in cultivars of wheat: growth temperature-dependent differential modulation of photosystem 1 and 2 activity and foliar antioxidant defense capacity. J. Plant Physiol. 159 : 49-59.
https://doi.org/10.1078/0176-1617-00594
 
45. Dat J.F., Lopez-Delgado H.L., Foyer C.H., Scott I.M. 1998. Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol. 116 : 1351-1357. Doi: https://doi.org/10.1104/pp.116.4.1351
https://doi.org/10.1104/pp.116.4.1351
 
46. Demidchik V. 2012. Reactive oxygen species and oxidative stress in plants. In: Plant Stress Physiology. Ed. S. Shabala. CAB International : 24-58.
https://doi.org/10.1079/9781845939953.0024
 
47. Ding X., Jiang Y., He L., Zhou Q., Yu J., Hui D., Huang D. 2016. Exogenous glutathione improves high root-zone temperature tolerance by modulating photosynthesis, antioxidant and osmolytes systems in cucumber seedlings. Sci Rep. 18 (6) : 35424. Doi: 10.1038/srep35424
https://doi.org/10.1038/srep35424
 
48. Divi U.K., Rahman T., Krishna P. 2010. Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biology. 10 : 151-164. Doi: 10.1186/1471-2229-10-151
https://doi.org/10.1186/1471-2229-10-151
 
49. Fahad Sh., Bajwa A.A. Nazir U., Anjum Sh.A., Farooq A., Zohaib A., Sadia S., Nasim W., Adkins S., Saud Sh., Ihsan M.Z., Alharby H., Wu Ch., Wang D., Huang J. 2017. Crop production under drought and heat stress: plant responses and management. Front Plant Sci. 8 : 1147. Doi: org/10.3389/fpls.2017.01147
https://doi.org/10.3389/fpls.2017.01147
 
50. Fancy N.N., Bahlmann A.K. Loake G.J. 2017. Nitric oxide function in plant abiotic stress. Plant Cell Environ. 40 : 462-472. doi: 10.1111/pce.12707
https://doi.org/10.1111/pce.12707
 
51. Ford P.C. 2010. Reactions of NO and nitrite with heme models and proteins. Inorg. Chem. 49 : 6226-6239. Doi: 10.1021/ic902073z
https://doi.org/10.1021/ic902073z
 
52. Freschi L. 2013. Nitric oxide and phytohormone interactions: current status and perspectives. Front. Plant Sci. 4 : 398. Doi: 10.3389/fpls.2013.00398
https://doi.org/10.3389/fpls.2013.00398
 
53. Gill S.S., Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48 : 909-930. Doi: 10.1016/j.plaphy.2010.08.016
https://doi.org/10.1016/j.plaphy.2010.08.016
 
54. Gould K.S., Lamotte O., Klinguer A., Pugin A.A., Wendehenne D. 2003. Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ. 26 : 1851-1862. Doi: org/10.1046/j.1365-3040.2003.01101.x
https://doi.org/10.1046/j.1365-3040.2003.01101.x
 
55. Gould K.S., Lister C. 2006. Flavonoid functions in plants. In: Flavonoids: chemistry, biochemistry, and applications. Eds. O.M. Andersen, K.R. Markham. Taylor & Francis Group : 397-442.
https://doi.org/10.1201/9781420039443.ch8
 
56. Hasanuzzaman M., Nahar K., Mahabub A. Fujita M. 2012. Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum L.) seedlings by modulating the antioxidant defense and glyoxalase system. Austr. J. Crop Sci. 6 : 1314-1323.
 
57. Hasanuzzaman M., Nahar K., Alam M.M., Roychowdhury R., Fujita M. 2013. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci. 14 : 9643-9684. Doi: 10.3390/ijms14059643
https://doi.org/10.3390/ijms14059643
 
58. Hayat S., Hasan S.A., Yusuf M., Hayat Q., Ahmad A. 2010. Effect of 28-homobrassinolide on photosynthesis, fluorescence and antioxidant system in the presence or absence of salinity and temperature in Vigna radiate. Environ. Exp. Bot. 69 : 105-112. Doi: org/10.1016/j.envexpbot.2010.03.004
https://doi.org/10.1016/j.envexpbot.2010.03.004
 
59. Hu X., Liu R., Li Y., Wang W., Tai F., Xue R., Li C. 2010. Heat shock protein 70 regulates the abscisic acid-induced antioxidant response of maize to combined drought and heat stress. Plant Growth Regul. 60 : 225-235. Doi: org/10.1007/s10725-009-9436-2
https://doi.org/10.1007/s10725-009-9436-2
 
60. Huang Y.W., Zhou Z.Q., Yang H.X., Wei C.X., Wan Y.Y., Wang X.J., Bai J.G. 2015. Glucose application protects chloroplast ultrastructure in heat-stressed cucumber leaves through modifying antioxidant enzyme activity. Biol. Plant. 59 : 131-138. Doi: org/10.1007/s10535-014-0470-1
https://doi.org/10.1007/s10535-014-0470-1
 
61. Inaba M., Suzuki I., Szalontai B., Kanesaki Y., Los D.A., Hayashi H., Murata N. 2003. Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in synechocystis. J Biol Chem. 278 : 12191-12198. Doi: 10.1074/jbc.M212204200
https://doi.org/10.1074/jbc.M212204200
 
62. Kagale S., Divi U.K., Krochko J.E., Keller W.A., Krishna P. 2007. Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta. 225 : 353-364. Doi: 10.1007/s00425-006-0361-6
https://doi.org/10.1007/s00425-006-0361-6
 
63. 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. doi: http://dx.doi.org/10.15407/ubj87.06.104
https://doi.org/10.15407/ubj87.06.104
 
64. Kimura S., Kaya H., Kawarazaki T., Hiraoka G., Senzaki E., Michikawa M., Kuchitsu K. 2012. Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochim. Biophys. Acta. 1823 : 398-405. Doi: 10.1016/j.bbamcr.2011.09.011
https://doi.org/10.1016/j.bbamcr.2011.09.011
 
65. Komayama K., Khatoon M., Takenaka D., Horie J., Yamashita A., Yoshioka M., Nakayama Y., Yoshida M., Ohira S., Morita N., Velitchkova M., Enami I., Yamamoto Y. 2007. Quality control of photosystem II: Cleavage and aggregation of heat-damage D1 protein in spinach thylakoids. Biochim. Biophys. Acta. 1767: 838-846. Doi: 10.1016/j.bbabio.2007.05.001
https://doi.org/10.1016/j.bbabio.2007.05.001
 
66. Koubouris G.C., Kavroulakis N., Metzidakis I.T., Vasilakakis M.D., Sofo A. 2015. Ultraviolet-B radiation or heat cause changes in photosynthesis, antioxidant enzyme activities and pollen performance in olive tree. Photosynthetica. 53 : 279-287. Doi: org/10.1007/s11099-015-0102-9
https://doi.org/10.1007/s11099-015-0102-9
 
67. Kumar R.R., Singh G.P., Sharma S.K., Singh K., Goswami S., Rai R.D. 2012b. Molecular cloning of HSP17 gene (sHSP) and their differential expression under exogenous putrescine and heat shock in wheat (Triticum aestivum). Afr. J. Biotechnol. 11 : 16800-16808.
 
68. Leshem Y.Y. 2001. Nitric Oxide in Plants. Occurance, Function and Use. Boston, MA : Kulwer Academic Publishers : 153 p.
 
69. Li Z.G., Yi X.Y., Li Y.T. 2014. Effect of pretreatment with hydrogen sulfide donor sodium hydrosulfide on heat tolerance in relation to antioxidant system in maize (Zea mays) seedlings. Biologia. 69 : 1001-1009. Doi: org/10.2478/s11756-014-0396-2
https://doi.org/10.2478/s11756-014-0396-2
 
70. Li B., Gao K., Ren H., Tang W. 2018. Molecular mechanisms governing plant responses to high temperatures. Invited Expert Review. Special Issue: Cell Signaling. doi: [10.1111/jipb.12701]
https://doi.org/10.1111/jipb.12701
 
71. Li, Z.G., Yang, S.Z., Long, W.B., Yang, G.X. Shen, Z.Z. 2013. Hydrogen sulfide 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. Doi: 10.1111/pce.12092.
https://doi.org/10.1111/pce.12092
 
72. Liao C., Zheng Y., Guo Y. 2017. MYB30 transcription factor regulates oxidative and heat stress responses through ANNEXIN-mediated cytosolic calcium signaling in Arabidopsis. New Phytol. 216 : 163-177. doi: 10.1111/nph.14679
https://doi.org/10.1111/nph.14679
 
73. Lisjak M., Teklic T., Wilson I.D., Whiteman M., Hancock J.T. 2013. Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ. 36 : 1607-1616.
https://doi.org/10.1111/pce.12073
 
74. Liu H.T., Li B., Shang Z.L., Li X.Z., Mu R.L., Sun D.Y., Zhou R.G. 2003. Calmodulin is involved in heat shock signal transduction in wheat. Plant Physiol. 132 : 1186-1195. Doi: https://doi.org/10.1104/pp.102.018564
https://doi.org/10.1104/pp.102.018564
 
75. Lopez-Delgado H., Dat J.F., Foyer C.H., Scott I.M. 1998. Induction of ther-motolerance in potato microplants by acetylsalicylic acid and H2O2. J. Exp. Bot. 49 : 713-720. Doi: org/10.1093/jxb/49.321.713
https://doi.org/10.1093/jexbot/49.321.713
 
76. Mazorra L.M., Holton N., Bishop G.J., Núñez M. 2011. Heat shock response in tomato brassinosteroid mutants indicates that thermotolerance is independent of brassinosteroid homeostasis. Plant Physiol. Biochem. 49: 1420-1428. Doi: 10.1016/j.plaphy.2011.09.005
https://doi.org/10.1016/j.plaphy.2011.09.005
 
77. Miller E.W., Dickinson B.C., Chang C.J. 2010. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc. Natl. Acad. Sci. USA. V. 107. P. 15681-15686. Doi: 10.1073/pnas.1005776107
https://doi.org/10.1073/pnas.1005776107
 
78. Moustaka J., Ouzounidou G., Sperdouli I., Moustakas M. 2018. Photosystem II is more sensitive tan photosystem I to Al3+ induced phytotoxicity. Materials (Basel). 11
https://doi.org/10.3390/ma11091772
 
(9) : 1772. DOI: 10.3390/ma11091772.
https://doi.org/10.3390/ma11091772
 
79. Niu Y., Xiang Y. 2018. An overview of biomembrane functions in plant responses to high-temperature stress. Front Plant Sci. 9 : 915. Doi: 10.3389/fpls.2018.00915
https://doi.org/10.3389/fpls.2018.00915
 
80. Oda T., Hashimoto H., Kuwabara N., Akashi S., Hayashi K., Kojima C., Wong H.L., Kawasaki T., Shimamoto K., Sato M., Shimizu T. 2010. Structure of the N-terminal regulatory domain of a plant NADPH oxidase and its functional implications // J. Biol. Chem. V. 285. P. 1435-1445. Doi: 10.1074/jbc.M109.05890
https://doi.org/10.1074/jbc.M109.058909
 
81. 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. Doi: 10.1074/jbc.M708106200
https://doi.org/10.1074/jbc.M708106200
 
82. Ogawa K., Kanematsu S., Asada K. 1997. Generation of superoxide anion and localisation of Cu/Zn-superoxide dismutase in vascular tissue of spinach hypocotyls: their association with lignification. Plant Cell Physiol. 38 : 1118-1126. Doi: 10.1093/oxfordjournals.pcp.a029096
https://doi.org/10.1093/oxfordjournals.pcp.a029096
 
83. Ogweno J. O., Song X.S., Shi K., Hu W.H., Mao W. H., Zhou Y.H. Yu J.Q., Nogues S. 2008. Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. J. Plant Growth Regul. 27 : 49-57. Doi: org/10.1007/s00344-007-9030-7
https://doi.org/10.1007/s00344-007-9030-7
 
84. Parankusam S., Adimulam S.S., Bhatnagar-Mathur P., Sharma K.K. 2017. Nitric oxide (NO) in plant heat stress tolerance: Current knowledge and perspectives. Front Plant Sci. 13 : 1582. Doi: 10.3389/fpls.2017.01582
https://doi.org/10.3389/fpls.2017.01582
 
85. Peng S., Huang J., Sheehy J.E., Laza R.C., Visperas R.M., Zhong X., Centeno G.S., Khush G.S., Cassman K.G. 2004. Rice yields decline with higher night temperature from global warming. Proc. Natl Acad. Sci. USA. 101 : 9971-9975. Doi: org/10.1073/pnas.0403720101
https://doi.org/10.1073/pnas.0403720101
 
86. Radi R. 2004. Nitric oxide, oxidants, and protein tyrosine nitration. Proc. Natl. Acad. Sci. 101 : 4003-4008. Doi: 10.1073/pnas.0307446101
https://doi.org/10.1073/pnas.0307446101
 
87. Sagi M., Fluhr R. 2006. Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol. 141 : 336-340. Doi: 10.1104/pp.106.078089
https://doi.org/10.1104/pp.106.078089
 
88. Sairam R.K., Srivastava G.C., Saxena D.C. 2000. Increased antioxidant activity under elevated temperatures: a mechanism of heat stress tolerance in wheat genotypes. Biol. Plant. 43 : 245-251.
https://doi.org/10.1023/A:1002756311146
 
89. Schmid-Siegert E., Stepushenko O., Glauser G., Farmer E.E. 2016. Membranes as structural antioxidants recycling of malondialdehyde to its source in oxidation-sensitive chloroplast fatty acids // J. Biol. Chem. 291 : 13005-13013. Doi: 10.1074/jbc.M116.729921
https://doi.org/10.1074/jbc.M116.729921
 
90. Sharkey T.D., Zhang R. 2010. High temperature effects on electron and proton circuits of photosynthesis. J. Integr. Plant Biol. 52 : 712-722. Doi: 10.1111/j.1744-7909.2010.00975.x
https://doi.org/10.1111/j.1744-7909.2010.00975.x
 
91. 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
 
92. Singh I., Shono M. 2005. Physiological and molecular effects of 24-epibrassinolide, a brassinosteroid on thermotolerance of tomato. Plant Growth Regul. 47 : 111-119. Doi: org/10.1007/s10725-005-3252-0
https://doi.org/10.1007/s10725-005-3252-0
 
93. 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. Doi: 10.1016/j.plantsci.2006.05.002
https://doi.org/10.1016/j.plantsci.2006.05.002
 
94. Stocker T. 2013. IPCC, 2013: Technical summary. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.
 
95. Sung D.Y., Kaplan F., Lee K.J., Guy C.L. 2003. Acguired tolerance to tem-perature extremes. Trends Plant Sci. 8 : 179-187. Doi: 10.1016/S1360-1385(03)00047-5
https://doi.org/10.1016/S1360-1385(03)00047-5
 
96. Suzuki N., Miller G., Salazar C., Mondal H.A., Shulaev E., Cortes D.F., Shuman J.L., Luo X., Shah J., Schlauch K., Shulaev V., Mittler R. 2013. Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell. 25 (9) : 3553-5369. doi: 10.1105/tpc.113.114595.
https://doi.org/10.1105/tpc.113.114595
 
97. Takeda T. Yokota A., Shigeoka S. 1995. Resistance of photosynthesis to hydrogen peroxide in algae. Plant Cell Physiol. 36 : 1089-1095. Doi: org/10.1093/oxfordjournals.pcp.a078852
https://doi.org/10.1093/oxfordjournals.pcp.a078852
 
98. Tian S., Wang X., Li P., Wang, H., Ji H., Xie J., Qiu Q., Shen D., Dong H. 2016. Plant aquaporin AtPIP1;4 links apoplastic H2O2 induction to disease immunity pathways. Plant Physiol. 171 : 1635-1650. Doi: 10.1104/pp.15.01237
https://doi.org/10.1104/pp.15.01237
 
99. Uchida A., Jagendorf A.T., Hibino 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. Doi: org/10.1016/S0168-9452(02)00159-0
https://doi.org/10.1016/S0168-9452(02)00159-0
 
100. Wilen R.W., Sacco M., Gusta L.V., Krishna P. 1995. Effects of 24-epibrassinolide on freezing and thermotolerance of bromegrass (Bromus inermis) cell cultures. Physiol. Plant. 95 : 195-202. Doi: org/10.1111/j.1399-3054.1995.tb00827.x
https://doi.org/10.1034/j.1399-3054.1995.950204.x
 
101. 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 Rac GTPase to its N-terminal extension. Plant Cell. 19: 4022-4034. Doi: 10.1105/tpc.107.055624
https://doi.org/10.1105/tpc.107.055624
 
102. Xu S., Li J., Zhang X., Wei H., Cui L. 2006. Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ. Exp. Bot. 56 : 274-285. Doi: org/10.1016/j.envexpbot.2005.03.002
https://doi.org/10.1016/j.envexpbot.2005.03.002
 
103. Yamamoto Y., Aminaka R., Yoshioka M., Khatoon M., Komayama K., Takenaka D., Yamashita A., Nijio N., Inagawa K., Morita N., Sasaki T., Yamamoto Y. 2008. Quality control of photosystem II: impact of light and heat stresses. Photosynth Res. 98 : 589-608. Doi: 10.1007/s11120-008-9372-4
https://doi.org/10.1007/s11120-008-9372-4
 
104. Yang M., Qin B.P., Ma X.L., Wang P., Li M.L., Chen L.L., Chen L.T., Sun A.Q., Wang Z.L., Yin Y.P. 2015. Foliar application of sodium hydrosulfide (NaHS), a hydrogen sulfide (H2S) donor, can protect seedlings against heat stress in wheat (Triticum aestivum L.). J. Integr. Agricult. 15 : 2745-2758. Doi: 10.1016/S2095-3119(16)61358-8
https://doi.org/10.1016/S2095-3119(16)61358-8
 
105. Yao Y., He R.J., Xie Q.L., Zhao X.H., Deng X.M., He J.B., Song L., He J., Marchant A., Chen X.Y., Wu A.M. 2017. ETHYLENE RESPONSE FACTOR 74 (ERF74) plays an essential role in controlling a respiratory burst oxidase homolog D (RbohD)-dependent mechanism in response to different stresses in Arabidopsis. New Phytol. 213 : 1667-1681. Doi: 10.1111/nph.14278
https://doi.org/10.1111/nph.14278
 
106. Yoshioka M. 2016. Quality control of photosystem ii: the mechanisms for avoidance and tolerance of light and heat stresses are closely linked to membrane fluidity of the thylakoids. Front Plant Sci. 7 : 1136. Doi: 10.3389/fpls.2016.01136.
https://doi.org/10.3389/fpls.2016.01136
 
107. Yu M., Lamattina L., Spoel S.H., Loake G.J. 2014. Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol. 202 : 1142-1156. Doi: 10.1111/nph.12739.
https://doi.org/10.1111/nph.12739