Цитологія і генетика 2019, том 53, № 5, 56-74
Cytology and Genetics 2019, том 53, № 5, 392–406, doi: https://www.doi.org//10.3103/S0095452719050098

Газотрансмиттеры и их роль в адаптивных реакциях растительных клеток

Колупаев Ю.Е., Карпец Ю.В., Бесчасный С.П., Дмитриев А.П.

  1. Харьковский национальный аграрный университет им. В.В. Докучаева, п/о Докучаевское-2, 62483, Харьков, Украина
  2. Харьковский национальный университет им. В.Н. Каразина, площадь Свободы, 4, 61022, Харьков, Украина
  3. Херсонский государственный университет, ул. Университетская, 27, 73000, Херсон, Украина
  4. Институт клеточной биологии и генетической инженерии НАН Украины, ул. Академика Заболотного, 148, 03143, Киев, Украина

Обзор посвящен физиологическим функциям основных газотрансмиттров (ГТ) у растений. Охарактеризованы пути синтеза оксида азота, сероводорода и монооксида углерода. Показано их взаимодействие (cross-talk) с другими ключевыми участниками сигналинга – ионами кальция и активными формами кислорода. Рассмотрены основные пути модификации ГТ целевых белков: S-нитрозилирование, нитрование, персульфидирование. Особое внимание уделено механизмам функционального взаимодействия ГТ между собой, обусловленным прямым химическим взаимодействием, конкуренцией за мишени биомакромолекул, взаимным влиянием на синтез. Описано участие эндогенных ГТ в процессах адаптации растений к действию основных абиотических стрессоров: низких и высоких температур, обезвоживания и засоления. Приведены примеры практического использования доноров ГТ для индуцирования устойчивости растений к абиотическим стрессам.

РЕЗЮМЕ. Огляд присвячений фізіологічним функціям основних газотрансмітерів (ГТ) у рослин. Охарактеризовані шляхи синтезу оксиду азоту, сірководню та монооксиду вуглецю. Показано їх взаємодію (cross-talk) з іншими ключовими учасниками сигналінгу – іонами кальцію та активними формами кисню. Розглянуто основні шляхи модифікації ГТ цільових білків: S-нітрозилювання, нітрування, персульфідування. Особливу увагу приділено механізмам функціональної взаємодії ГТ між собою, зумовленим прямою хімічною взаємодією, конкуренцією за мішені біомакромолекул, взаємним впливом на синтез. Описано участь ендогенних ГТ в процесах адаптації рослин до дії основних абіотичних стресорів: низьких і високих температур, зневоднення і засолення. Наведені приклади практичного використання донорів ГТ для індукування стійкості рослин до абіотичних стресів.

Ключові слова: оксид азота (NO), сероводород (H2S), монооксид углерода (CO), активные формы кислорода, кальций, функциональное взаимодействие газотрансмиттеров, адаптивные реакции растений

Цитологія і генетика
2019, том 53, № 5, 56-74

Current Issue
Cytology and Genetics
2019, том 53, № 5, 392–406,
doi: /10.3103/S0095452719050098

Повний текст та додаткові матеріали

Цитована література

1. Peers, C. and Lefer, D.J., Emerging roles for gasotransmitters, Exp. Physiol., 2011, vol. 96, no. 9, pp. 831–832. https://doi.org/10.1113/expphysiol.2011.057422

2. Sukmansky, O.I. and Reutov, V.P., Gasotransmitters: physiological role and involvement in the pathogenesis of the diseases, Usp. Fiziol. Nauk, 2016, vol. 47, no. 3, pp. 30–58.

3. He, H. and He, L., The role of carbon monoxide signaling in the responses of plants to abiotic stresses, Nitric Oxide, 2014, vol. 42, pp. 40–43. https://doi.org/10.1016/j.niox.2014.08.011

4. Khan M.N., Mobin M., Abbas Z.K. Nitric oxide and high temperature stress: A physiological perspective, in Nitric Oxide Action in Abiotic Stress Responses in Plants, Khan, M.N., Eds., Switzerland: Springer, 2015, pp. 77–93. https://doi.org/10.1007/978-3-319-17804-2_5

5. Wang, R., Gasotransmitters: growing pains and joys, Trends Biochem. Sci., 2014, vol. 39, no. 5, pp. 227–232. https://doi.org/10.1016/j.tibs.2014.03.003

6. Yamasaki, H. and Cohen, M.F., Biological consilience of hydrogen sulfide and nitric oxide in plants: gases of primordial earth linking plant, microbial and animal physiologies, Nitric Oxide, 2016, vols. 55–56, pp. 91–100. https://doi.org/10.1016/j.niox.2016.04.002

7. Lamattina, L. and Garcia-Mata, C., Preface, in Gasotransmitters in Plants, Signaling and Communication in Plants, Lamattina, L. and Garcia-Mata, C., Eds., Switzerland: Springer, 2016, pp. v–ix. https://doi.org/10.1007/978-3-319-40713-5

8. Correa-Aragunde, N., Graziano, M., and Lamattina, L., Nitric oxide plays a central role in determining lateral root development in tomato, Planta, 2004, vol. 218, no. 6, pp. 900–917. https://doi.org/10.1007/s00425-003-1172-7

9. Wilson, I.D., Neill, S.J., and Hancock, J.T., Nitric oxide synthesis and signaling in plants, Plant Cell Environ., 2008, vol. 31, no. 5, pp. 622–631. https://doi.org/10.1111/j.1365-3040.2007.01761.x

10. Krasylenko, Y.A., Yemets, A.I., and Blume, Y.B., Functional role of nitric oxide in plants. Russ. J. Plant Physiol., 2010, vol. 57, no. 4, pp. 451–461. https://doi.org/10.1134/S1021443710040011

11. Vasil’eva G.G. Reactive oxygen and nitrogen species in legume-rhizobial symbiosis: a review, Appl. Biochem. Microbiol., 2010, vol. 46, no. 1, pp. 15–22. https://doi.org/10.1134/S0003683810010023

12. del Giudice, J., Cam, Y., Damiani, I., Fung-Chat, F., Meilhoc, E., Bruand, C., Brouquisse, R., Puppo, A., and Boscari, A., Nitric oxide is required for an optimal establishment of the Medicago truncatula, Sinorhizobium meliloti symbiosis, New Phytol., 2011, vol. 191, no. 2, pp. 405–417. https://doi.org/10.1111/j.1469-8137.2011.03693.x

13. Mamaeva, A.S., Fomenkov, A.A., Nosov, A.V., Moshkov, I.E., Novikova, G.V., Mur, L.A.J., and Hall, M.A., Regulatory role of nitric oxide in plants, Russ. J. Plant Physiol., 2015, vol. 62, no. 4, pp. 427–440. https://doi.org/10.1134/S1021443715040135

14. Jin Q., Cui W., Xie Y., Shen W. Carbon monoxide: A ubiquitous gaseous signaling molecule in plants, in Gasotransmitters in Plants, Signaling and Communication in Plants, Lamattina, L. and Garcia-Mata, C., Eds., Switzerland: Springer, 2016, pp. 3–19. https://doi.org/10.1007/978-3-319-40713-5_1

15. Banerjee, A., Tripathi, D.K., and Roychoudhury, A., Hydrogen sulphide trapeze: environmental stress amelioration and phytohormone crosstalk, Plant Physiol. Biochem., 2018, vol. 132, pp. 46–53. https://doi.org/10.1016/j.plaphy.2018.08.028

16. Yemets A.I., Krasylenko Y.A., Blume Y.B. Nitric oxide and UV-B radiation, in Nitric Oxide Action in Abiotic Stress Responses in Plants, Khan, M.N., et al., Eds., Switzerland: Springer, 2015, pp. 141–154. https://doi.org/10.1007/978-3-319-17804-2_9

17. Hancock, J.T., Hydrogen sulfide and environmental stresses, Environ. Exp. Bot., 2018. https://doi.org/10.1016/j.envexpbot.2018.08.034

18. Durner, J., Wendehemme, D., and Klessig, D.F., Defense gene induction in tobacco by nitric oxide, cyclic GMP and cyclic ADP-ribose, Proc. Natl. Acad. Sci. U. S. A., 1998, vol. 95, pp. 10328–10333.

19. Corpas, F.J. and Barroso, J.B., Nitric oxide synthase like activity in higher plants, Nitric Oxide, 2017, vol. 68, pp. 5–6. https://doi.org/10.1016/j.niox.2016.10.009

20. Gupta, K.J. and Kaiser, W.M., Production and scavenging of nitric oxide by barley root mitochondria, Plant Cell Physiol., 2010, vol. 51, no. 4, pp. 576–584.

21. Farnese, F.S., Menezes-Silva, P.E., Gusman, G.S., and Oliveira, J.A., 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., 2016, vol. 7, p. 471. https://doi.org/10.3389/fpls.2016.00471

22. Neill, S., Barros, R., Bright, J., Desikan, R., Hancock, J., Harrison, J., Morris, P., Ribeiro, D., and Wilson, I., Nitric oxide, stomatal closure and abiotic stress, J. Exp. Bot., 2008, vol. 59, no. 2, pp. 165–176. https://doi.org/10.1093/jxb/erm293

23. Corpas, F.J., Palma, J.M., Sandalio, L.M., Valderrama, R., Barroso, J.B., and Del Rio, L.A., Peroxisomal xanthine oxidoreductase:characterization of the enzyme from pea (Pisum sativum L.) leaves, J. Plant Physiol., 2008, vol. 165, no. 13, pp. 1319–1330. https://doi.org/10.1016/j.jplph.2008.04.004

24. Flores, T., Todd, C.D., Tovar-Mendez, A., Dhanoa, P.K., Correa-Aragunde, N., Hoyos, M.E., Brownfield, D.M., Mullen, R.T., Lamattina, L., and Polacco, J.C., Arginase-negative mutants of Arabidopsis exhibit increased nitric oxide signaling in root development, Plant Physiol., 2008, vol. 147, no. 4, pp. 1936–1946. https://doi.org/10.1104/pp.108.121459

25. Saha, J., Brauer, E.K., Sengupta, A., Popescu, S.C., Gupta, K., and Gupta, B., Polyamines as redox homeostasis regulators during salt stress in plants, Front. Environ. Sci., 2015, vol. 3, p. 21. https://doi.org/10.3389/fenvs.2015.00021

26. Rumer, S., Gupta, K.J., and Kaiser, W.M., Plant cells oxidize hydroxylamines to NO, J. Exp. Bot., 2009, vol. 60, pp. 2065–2072. https://doi.org/10.1093/jxb/erp077

27. Romero, L.C., Garcia, I., and Gotor, C., L-cysteine desulfhydrase 1 modulates the generation of the signaling molecule sulfide in plant cytosol., Plant Signal. Behav., 2013, vol. 8, no. 5, pp. 4621–4634. https://doi.org/10.4161/psb.24007

28. Li, Z.G., Chapter Thirteen: analysis of some enzymes activities of hydrogen sulfide metabolism in plants, Methods Enzymol., 2015, vol. 555, pp. 253–269. https://doi.org/10.1016/bs.mie.2014.11.035

29. Li, Z.-G., Min, X., and Zhou, Z.-H., Hydrogen sulfide: a signal molecule in plant cross-adaptation, Front. Plant Sci., 2016, vol. 7, p. 1621. https://doi.org/10.3389/fpls.2016.01621

30. Zhang, H., Hydrogen sulfide in plant biology, in Gasotransmitters in Plants. Signaling and Communication in Plants, Lamattina, L. and Garcia-Mata, C., Eds., Switzerland: Springer, 2016, pp. 23–51. https://doi.org/10.1007/978-3-319-40713-5_2

31. Li, Z.G., Hydrogen sulfide: a multifunctional gaseous molecule in plants, Russ. J. Plant Physiol., 2013, vol. 60, no. 6, pp. 733–740. https://doi.org/10.1134/S1021443713060058

32. Wirtz, M. and Hell, R., Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties, J. Plant Physiol., 2006, vol. 163, no. 3, pp. 273–286. https://doi.org/10.1016/j.jplph.2005.11.013

33. Rudenko, N.N., Ignatova, L.K., Fedorchuk, T.P., and Ivanov, B.N., Carbonic anhydrases in photosynthetic cells of higher plants. Biochemistry (Moscow), 2015, vol. 80, no. 6, pp. 674–687. https://doi.org/10.1134/S0006297915060048

34. Silva, C.J. and Modolo, L.V., Hydrogen sulfide: a new endogenous player in an old mechanism of plant tolerance to high salinity, Acta Bot. Brasil., 2018, vol. 32, no. 1, pp. 150–160. https://doi.org/10.1590/0102-33062017abb0229

35. Roszer, T., Biosynthesis of nitric oxide in plants, in Nitric Oxide in Plants: Metabolism and Role in Stress Physiology, Khan, M.N., et al., eds., Switzerland: Springer, 2014, pp. 17–32. https://doi.org/10.1007/978-3-319-06710-0_2

36. Crawford, N.M., Mechanisms for nitric oxide synthesis in plants, J. Exp. Bot., 2006, vol. 57, no. 3, pp. 471–478. https://doi.org/10.1093/jxb/erj050

37. Rosales, E.P., Iannone, M.F., Groppa, M.D., and Benavides, M.P., Polyamines modulate nitrate reductase activity in wheat leaves: involvement of nitric oxide, Amino Acids, 2012, vol. 42, nos. 2–3, pp. 857–865. https://doi.org/10.1007/s00726-011-1001-4

38. Rosales, E.P., Iannone, M.F., Groppa, M.D., and Benavides, M.P., Nitric oxide inhibits nitrate reductase activity in wheat leaves, Plant Physiol. Biochem., 2011, vol. 49, no. 2, pp. 124–130. https://doi.org/10.1016/j.plaphy.2010.10.009

39. Karpets, Yu.V., Kolupaev, Yu.E., Lugovaya, A.A., Shvidenko, N.V., and Yastreb, T.O., Effects of nitrate and L-arginine on content of nitric oxide and activities of antioxidant enzymes in roots of wheat seedlings and their heat resistance, Russ. J. Plant Physiol., 2018, vol. 65, no. 6, pp. 908–915. https://doi.org/10.1134/S1021443718050096

40. Gupta, K.J., Fernie, A.R., Kaiser, W.M., and van Dongen, J.T., On the origins of nitric oxide, Trends Plant Sci., 2011, vol. 16, no. 3, pp. 160–168. https://doi.org/10.1016/j.tplants.2010.11.007

41. Freschi, L., Nitric oxide and phytohormone interactions: current status and perspectives, Front. Plant Sci., 2013, vol. 4, p. 398. https://doi.org/10.3389/fpls.2013.00398

42. Abe, K. and Kimura, H., The possible role of hydrogen sulfide as an endogenous neuromodulator, J. Neurosci., 1996, vol. 16, pp. 1066–1071.

43. Lisjak, M., Teklic, T., Wilson, I.D., Whiteman, M., and Hancock, J.T., Hydrogen sulfide: environmental factor or signalling molecule?, Plant Cell Environ., 2013, vol. 36, no. 9, pp. 1607–1616. https://doi.org/10.1111/pce.12073

44. Verma, A., Hirsch, D.J., Glatt, C.E., Ronnett, G.V., and Snyder, S.H., Carbon monoxide: a putative neural messenger, Science, 1993, vol. 259, pp. 381–384.

45. Wilks, S.S., Carbon monoxide in green plants, Science, 1959, vol. 129, pp. 964–966.

46. Gisk, B., Yasui, Y., Kohchi, T., and Frankenberg-Dinkel, N., Characterization of the haem oxygenase protein family in Arabidopsis thaliana reveals a diversity of functions, Biochem. J., 2010, vol. 425, no. 2, pp. 425–434. https://doi.org/10.1042/BJ20090775

47. Bauer, M., Huse, K., Settmacher, U., and Claus, R.A., The heme oxygenase-carbon monoxide system: regulation and role in stress response and organ failure, Intensive Care Med., 2008, vol. 34, no. 4, pp. 640–648. https://doi.org/10.1007/s00134-008-1010-2

48. Emborg, T.J., Walker, J.M., Noh, B., and Vierstra, R.D., Multiple heme oxygenase family members contribute to the biosynthesis of the phytochrome chromophore in Arabidopsis, Plant Physiol., 2006, vol. 140, no. 3, pp. 856–868. https://doi.org/10.1104/pp.105.074211

49. Zilli, C.G., Balestrasse, K.B., Yannarelli, G.G., Polizio, A.H., Santa-Crutz, D.M., and Tomaro, M.L., Heme oxygenase up-regulation under salt stress protects nitrogen metabolism in nodules of soybean plants, Environ. Exp. Bot., 2008, vol. 64, pp. 83–89. https://doi.org/10.1016/j.envexpbot.2008.03.005

50. Ludidi, N. and Gehring, C., Identification of a novel protein with guanylyl cyclase activity in Arabidopsis thaliana, J. Biol. Chem., 2003, vol. 278, pp. 6490–94.

51. Baudouin, E., The language of nitric oxide signaling, Plant Biol. (Stuttg.), 2011, vol. 13, no. 2, pp. 233–242. https://doi.org/10.1111/j.1438-8677.2010.00403.x

52. Lamotte, O., Guold, K., Lecourieux, D., Sequeira-Legrand, A., Lebrun-Garcia, A., Durner, J., Pugin, A., and Wendehenne, D., Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein, Plant Physiol., 2004, vol. 135, pp. 516–529. https://doi.org/10.1104/pp.104.038968

53. Kolupaev, Yu.E., Karpets, Yu.V., and Dmitriev, A.P., Signal mediators in plants in response to abiotic stress: calcium, reactive oxygen and nitrogen species, Cytol. Genet., 2015, vol. 49, no. 5, pp. 338–348. https://doi.org/10.3103/S0095452715050047

54. Karpets, Yu.V., Kolupaev, Yu.E., Yastreb, T.O., and Oboznyi, A.I., 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., 2016, vol. 63, no. 4, pp. 490–498. https://doi.org/10.1134/S1021443716040075

55. Astier, J. and Lindermayr, C., Nitric oxide-dependent posttranslational modification in plants: an update, Int. J. Mol. Sci., 2012, vol. 13, no. 11, pp. 15193–15208. https://doi.org/10.3390/ijms131115193

56. Arora, D., Jain, P., Singh, N., Kaur, H., and Bhatla, S.C., Mechanisms of nitric oxide crosstalk with reactive oxygen species scavenging enzymes during abiotic stress tolerance in plants, Free Radical Res., 2016, vol. 50, no. 3, pp. 291–303. https://doi.org/10.3109/10715762.2015.1118473

57. Kaur, K. and Kaur, K., Nitric oxide improves thermotolerance in spring maize by inducing varied genotypic defense mechanisms, Acta Physiol. Plant., 2018, vol. 40, p. 55. https://doi.org/10.1007/s11738-018-2632-9

58. Guo, H., Xiao, T., Zhou, H., Xie, Y., and Shen, W., Hydrogen sulfide: a versatile regulator of environmental stress in plants, Acta Physiol. Plant., 2016, vol. 38, p. 16. https://doi.org/10.1007/s11738-015-2038-x

59. Cuevasanata, E., Lange, M., Bonanata, J., Coitino, E.L., Ferrer-Sueta, G., Filipovic, M.R., and Alvarez, B., Reaction of hydrogen sulphide with disulfide and sulfenic acid to form the strongly nucleophilic persulfide, J. Biol. Chem., 2015, vol. 290, no. 45, pp. 26866–26880. https://doi.org/10.1074/jbc.M115.672816

60. Kolupaev, Yu.E., Firsova, E.N., Yastreb, T.O., and Lugovaya, A.A., 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., 2017, vol. 53, no. 5, pp. 573–579. https://doi.org/10.1134/S0003683817050088

61. Li, Z.G., Yi, X.Y., and Li, Y.T., Effect of pretreatment with hydrogen sulfide donor sodium hydrosulfide on heat tolerance in relation to antioxidant system in maize (Zea mays) seedlings, Biologia, 2014, vol. 69, no. 8, pp. 1001–1009. https://doi.org/10.2478/s11756-014-0396-2

62. Wang, L., Hou, Z., Hou, L., Zhao, F., and Liu, X., H2S induced by H2O2 mediates drought-induced stomatal closure in Arabidopsis thaliana, Chin. Bull. Bot., 2012, vol. 47, no. 3, pp. 217–225.

63. Shan, C., Zhang, S., and Ou, X., The roles of H2S and H2O2 in regulating AsA-GSH cycle in the leaves of wheat seedlings under drought stress, Protoplasma, 2018, vol. 255, no. 4, pp. 1257–62. https://doi.org/10.1007/s00709-018-1213-5

64. Fang, H.H., Pei, Y.X., Tian, B.H., Zhang, L.P., Qiao, Z.J., and Liu, Z.Q., Ca2+ participates in H2S-induced Cr6+ tolerance in Setaria italic, Chin. J. Cell Biol., 2014, vol. 36, pp. 758–765.

65. Yastreb, T.O., Kolupaev, Yu.E., Havva, E.N., Shkliarevskyi, M.A., and Dmitriev, A.P., Calcium and components of lipid signaling in implementation of hydrogen sulfide influence on state of stomata in Arabidopsis thaliana, Cytol. Genet., 2019, vol. 53, no. 2, pp. 99–105. https://doi.org/10.3103/S0095452719020099

66. Jin, Z., Xue, S., Luo, Y., Tian, B., Fang, H., Li, H., and Pei, Y., Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis, Plant Physiol. Biochem., 2013, vol. 62, pp. 41–46. https://doi.org/10.1016/j.plaphy.2012.10.017

67. Cao, Z., Huang, B., Wang, Q., Xuan, W., Ling, T., Zhang, B., Chen, X., Nie, L., and Shen, W., Involvement of carbon monoxide produced by heme oxygenase in ABA-induced stomatal closure in Vicia faba and its proposed signal transduction pathway, Chin. Sci. Bull., 2007, vol. 52, no. 17, pp. 2365–2373. https://doi.org/10.1007/s11434-007-0358-y

68. Xuan, W., Huang, L., Li, M., Huang, B., Xu, S., Hui, Y., Gao, L., and Shen, W., Induction of growth elongation in wheat root segments by heme molecules: a regulatory role of carbon monoxide in plants?, Plant Growth Regul., 2007, vol. 52, p. 41. https://doi.org/10.1007/s10725-007-9175-1

69. Sa, Z.S., Huang, L.Q., Wu, G.L., Ding, J.P., Chen, X.Y., Yu, T., Ci, S., and Shen, W.B., Carbon monoxide: a novel antioxidant against oxidative stress in wheat seedling leaves, J. Integr. Plant Biol., 2007, vol. 49, pp. 638–645. https://doi.org/10.1111/j.1744-7909.2007.00461.x

70. She, X.-P. and Song, X.-G., Carbon monoxide-induced stomatal closure involves generation of hydrogen peroxide in Vicia faba guard cells, J. Integr. Plant Biol., 2008, vol. 50, no. 12, pp. 1539–1548.

71. Williams, S.E., Wootton, P., Mason, H.S., Bould, J., Iles, D.E., Riccardi, D., Peers, C., and Kemp, P.J., Hemoxygenase-2 is an oxygen sensor for a calciumsensitive potassium channel, Science, 2004, vol. 306, pp. 2093–2097. https://doi.org/10.1126/science.1105010

72. Hsu, Y.Y., Chao, Y.Y., and Kao, C.H., Cobalt chloride-induced lateral root formation in rice: the role of heme oxygenase, J. Plant Physiol., 2013, vol. 170, no. 12, pp. 1075–1081. https://doi.org/10.1016/j.jplph.2013.03.004

73. Carballal, S., Trujillo, M., Cuevasanta, E., Bartesaghi, S., Möller, M.N., Folkes, L.K., García-Bereguiaín, M.A., Gutierrez-Merino, C., Wardman, P., Denicola, A., Radi, R., and Alvarez, B., Reactivity of hydrogen sulfide with peroxynitrite and other oxidants of biological interest, Free Radic. Biol. Med., 2011, vol. 50, no. 1, pp. 196–205. https://doi.org/10.1016/j.freeradbiomed.2010.10.705

74. Whiteman, M., Li, L., Kostetski, I., Chu, S.H., Siau, J.L., Bhatia, M., and Moore, P.K., Evidence for the formation of a novel nitrosothiol from the gaseous mediators nitric oxide and hydrogen sulphide, Biochem. Biophys. Res. Commun., 2006, vol. 343, no. 1, pp. 303–310. https://doi.org/10.1016/j.bbrc.2006.02.154

75. Tanou, G., Filippou, P., Belghazi, M., Job, D., Diamantidis, G., Fotopoulos, V., and Molassiotis, A., Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress, Plant J., 2012, vol. 72, no. 4, pp. 585–599. https://doi.org/10.1111/j.1365-313X.2012.05100.x

76. Sun, C., Shi, Z.-Z., Zhou, X., Chen, L., and Zhao, X.-M., Prediction of S-glutathionylation sites based on protein sequences, PLoS One, 2013, vol. 8. e55512. https://doi.org/10.1371/journal.pone.0055512

77. Hancock, J.T., Henson, D., Nyirenda, M., Desikan, R., Harrison, J., Lewis, M., Hughes, J., and Neill, S.J., Proteomic identification of glyceraldehyde 3-phosphate dehydrogenase as an inhibitory target of hydrogen peroxide in Arabidopsis, Plant Physiol. Biochem., 2005, vol. 43, no. 9, pp. 828–835. https://doi.org/10.1016/j.plaphy.2005.07.012

78. Aroca, A., Schneider, M., Scheibe, R., Gotor, C., and Romero, L.C., Hydrogen sulfide regulates the cytosolic/nuclear partitioning of glyceraldehyde-3-phosphate dehydrogenase by enhancing its nuclear localization, Plant Cell Physiol., 2017, vol. 58, no. 6, pp. 983–992. https://doi.org/10.1093/pcp/pcx056

79. Li, Z.G., Yang, S.Z., Long, W.B., Yang, G.X., and Shen, Z.Z., Hydrogen sulfide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings, Plant Cell Environ., 2013, vol. 36, no. 8, pp. 1564–1572. https://doi.org/10.1111/pce.12092

80. Silva, C.J., Mollica, D.C.F., Vicente, M.H., Peres, L.E.P., and Modolo, L.V., NO, hydrogen sulfide does not come first during tomato response to high salinity, Nitric Oxide, 2018, vol. 76, pp. 164–173. https://doi.org/10.1016/j.niox.2017.09.008

81. Wang, Y., Li, L., Cui, W., Xu, S., Shen, W., and Wang, R., Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway, Plant Soil, 2012, vol. 351, nos. 1–2, pp. 107–119. https://doi.org/10.1007/s11104-011-0936-2

82. Singh, V.P., Singh, S., Kumar, J., and Prasad, S.M., Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate–glutathione cycle: possible involvement of nitric oxide, J. Plant Physiol., 2015, vol. 181, pp. 20–29. https://doi.org/10.1016/j.jplph.2015.03.015

83. Karpets, Yu.V., Kolupaev, Yu.E., Yastreb, T.O., Horielova, O.I., Shklyarevskyi, M.A., and Dmitriev, O.P., Role of reactive oxygen and nitrogen species in the induction of heat resistance of wheat plantlets by exogenous hydrogen sulfide, Dopov. Nac. akad. nauk Ukr., 2019, no. 3, pp. 89–97. https://doi.org/10.15407/dopovidi2019.03.089

84. Hu, K.D., Tang, J., Zhao, D.L., Hu, L.Y., Li, Y.H., Liu, Y.S., Jones, R., and Zhang, H., Stomatal closure in sweet potato leaves induced by sulfur dioxide involves H2S and NO signaling pathways, Biol. Plant., 2014, vol. 58, no. 4, pp. 676–680. https://doi.org/10.1007/s10535-014-0440-7

85. Honda, K., Yamada, N., Yoshida, R., Ihara, H., Sawa, T., Akaike, T., and Iwai, S., 8-Mercapto-Cyclic GMP mediates hydrogen sulfide-induced stomatal closure in Arabidopsis, Plant Cell Physiol., 2015, vol. 56, no. 8, pp. 1481–1489. https://doi.org/10.1093/pcp/pcv069

86. Scuffi, D., Alvarez, C., Laspina, N., Gotor, C., Lamattina, L., and Garcia-Mata, C., Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure, Plant Physiol., 2014, vol. 166, no. 4, pp. 2065–2076. https://doi.org/10.1104/pp.114.245373

87. Song, X.G., She, X.P., and Zhang, B., Carbon monoxide-induced stomatal closure in Vicia faba is dependent on nitric oxide synthesis, Physiol. Plant., 2008, vol. 132, no. 4, pp. 514–525. https://doi.org/10.1111/j.1399-3054.2007.01026.x

88. Cao, Z., Xuan, W., Liu, Z., Li, X., Zhao, N., Xu, P., Wang, Z., Guan, R., and Shen, W., Carbon monoxide promotes lateral root formation in rapeseed, J. Integr. Plant Biol., 2007, vol. 49, pp. 1070–1079. https://doi.org/10.1111/j.1672-9072.2007.00482.x

89. Xie, Y., Ling, T., Han, Y., Liu, K., Zheng, Q., Huang, L., Yuan, X., He, Z., Hu, B., Fang, L., Shen, Z., Yang, Q., and Shen, W., Carbon monoxide enhances salt tolerance by nitric oxide-mediated maintenance of ion homeostasis and up-regulation of antioxidant defence in wheat seedling roots, Plant Cell Environ., 2008, vol. 31, no. 12, pp. 1864–1881. https://doi.org/10.1111/j.1365-3040.2008.01888.x

90. Han, Y., Qin, J., Chang, X.Z., Yang, Z.X., and Du, J.B., Hydrogen sulphide and carbon monoxide are in synergy with each other in the pathogenesis of recurrent febrile seizures, Cell Mol. Neurobiol., 2006, vol. 26, no. 1, pp. 101–107. https://doi.org/10.1007/s10571-006-8848-z

91. Lin, Y., Li, M., Cui, W., Lu, W., and Shen, W., Haem oxygenase-1 is involved in hydrogen sulfide-induced cucumber adventitious root formation, J. Plant Growth Regul., 2012, vol. 31, no. 4, pp. 519–528. https://doi.org/10.1007/s00344-012-9262-z

92. Li, Z.-G. and Gu, S.-P., Hydrogen sulfide as a signal molecule in hematin-induced heat tolerance of tobacco cell suspension, Biol. Plant., 2016, vol. 60, no. 3, pp. 595–600. https://doi.org/10.1007/s10535-016-0612-8

93. Zhao, M.G., Chen, L., Zhang, L.L., and Zhang, W.H., Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis, Plant Physiol., 2009, vol. 151, no. 2, pp. 755–767. https://doi.org/10.1104/pp.109.140996

94. Ziogas, V., Tanou, G., Filippou, P., Diamantidis, G., Vasilakakis, M., Fotopoulos, V., and Molassiotis, A., Nitrosative responses in citrus plants exposed to six abiotic stress conditions, Plant Physiol. Biochem., 2013, vol. 68, pp. 118–126. https://doi.org/10.1016/j.plaphy.2013.04.004

95. Puyaubert, J. and Baudouin, E., New clues for a cold case: nitric oxide response to low temperature, Plant Cell Environ., 2014, vol. 37, no. 12, pp. 2623–2630. https://doi.org/10.1111/pce.12329

96. Baudouin, E. and Jeandroz, S., Nitric oxide as a mediator of cold stress response: a transcriptional point of view, in Nitric Oxide Action in Abiotic Stress Responses in Plants, Khan, M.N., Eds., Switzerland: Springer, 2015, pp. 129–139. https://doi.org/10.1007/978-3-319-17804-2_8

97. Fancy, N.N., Bahlmann, A.K., and Loake, G.J., Nitric oxide function in plant abiotic stress, Plant Cell Environ., 2017, vol. 40, no. 4, pp. 462–472. https://doi.org/10.1111/pce.12707

98. Oz, M.T., Eyidogan, F., Yucel, M., and Oktem, H.A., Functional role of nitric oxide under abiotic stress conditions, in Nitric Oxide Action in Abiotic Stress Responses in Plants, Khan, M.N., Eds., Switzerland: Springer, 2015, pp. 21–42. https://doi.org/10.1007/978-3-319-17804-2_2

99. Sehrawat, A. and Deswal, R., S-Nitrosylation analysis in Brassica juncea apoplast highlights the importance of nitric oxide in cold-stress signaling, J. Proteome, 2014, vol. 13, no. 5, pp. 2599–2619. https://doi.org/10.1021/pr500082u

100. Fan, J., Chen, K., Amombo, E., Hu, Z., Chen, L., and Fu, J., Physiological and molecular mechanism of nitric oxide (NO) involved in bermudagrass response to cold stress, PLoS One, 2015, vol. 10, no. 7. e0132991. https://doi.org/10.1371/journal.pone.0132991

101. Sami, F., Faizan, M., Faraz, A., Siddiqui, H., Yusuf, M., and Hayat, S., Nitric oxidemediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress, Nitric Oxide, 2018, vol. 73, pp. 22–38. https://doi.org/10.1016/j.niox.2017.12.005

102. Fu, P.N., Wang, W.J., Hou, L.X., and Liu, X., Hydrogen sulfide is involved in the chilling stress response in Vitis vinifera L., Acta Soc. Bot. Pol., 2013, vol. 82, no. 4, pp. 295–302. https://doi.org/10.5586/asbp.2013.031

103. Du, X., Jin, Z., Liu, D., Yang, G., and Pei, Y., Hydrogen sulfide alleviates the cold stress through MPK4 in Arabidopsis thaliana, Plant Physiol. Biochem., 2017, vol. 120, pp. 112–119. https://doi.org/10.1016/j.plaphy.2017.09.028

104. Shi, H., Ye, T., and Chan, Z., Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L.). Pers.), Plant Physiol. Biochem., 2013, vol. 71. pp. 226–234. https://doi.org/10.1016/j.plaphy.2013.07.021

105. Kolupaev, Yu.E., Horielova, E.I., Yastreb, T.O., Popov, Yu.V., and Ryabchun, N.I., Phenylalanine ammonialyase activity and content of flavonoid compounds in wheat seedlings at the action of hypothermia and hydrogen sulfide donor, Ukr. Biochem. J., 2018, vol. 90, no. 6, pp. 12–20. https://doi.org/10.15407/ubj90.06.012

106. He, H. and He, L.F., Regulation of gaseous signaling molecules on proline metabolism in plants, Plant Cell Rep., 2018, vol. 37, no. 3, pp. 387–392. https://doi.org/10.1007/s00299-017-2239-4

107. Yu, M., Lamattina, L., Spoel, S.H., and Loake, G.J., Nitric oxide function in plant biology: a redox cue in deconvolution, New Phytol., 2014, vol. 202, no. 4, pp. 1142–1156. https://doi.org/10.1111/nph.12739

108. Christou, A., Filippou, P., Manganaris, G.A., and Fotopoulos, V., Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin, BMC Plant Biol., 2014, vol. 14, p. 42. https://doi.org/10.1186/1471-2229-14-42

109. Parankusam, S., Adimulam, S.S., Bhatnagar-Mathur, P., and Sharma, K.K., Nitric oxide (NO) in plant heat stress tolerance: current knowledge and perspectives, Front Plant Sci., 2017, vol. 13, no. 8, p. 1582. https://doi.org/10.3389/fpls.2017.01582

110. Karpets, Yu.V., Kolupaev, Yu.E., and Vayner, 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. https://doi.org/10.1134/S1021443714060090

111. Hasanuzzaman, M., Nahar, K., Mahabub, A., and Fujita, M., 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., 2012, vol. 6, pp. 1314–1323.

112. Kumar, R.R., Tasleem, M., Jain, M., Ahuja, S., Goswami, S., Bakshi, S., Jambhulkar, S., Singh, S.D., Singh, G.P., Pathak, H., Viswanathan, C., and Praveen, S., Nitric oxide triggered defense network in wheat: Augmenting tolerance and grain-quality related traits under heat-induced oxidative damage, Environ. Exp. Bot., 2019, vol. 158, pp. 189–204. https://doi.org/10.1016/j.envexpbot.2018.11.016

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

114. Cheng, T., Shi, J., Dong, Y., Ma, Y., Peng, Y., Hu, X., and Chen, J., 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., 2018, vol. 84, no. 1, pp. 11–23. https://doi.org/10.1007/s10725-017-0316-x

115. 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., and Yin, Y.P., 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., 2015, vol. 15, no. 12, pp. 2745–2758. https://doi.org/10.1016/S2095-3119(16)61358-8

116. Sang, J., Jiang, M., Lin, F., Xu, S., Zhang, A., and Tan, M., Nitric oxide reduces hydrogen peroxide accumulation involved in water stress-induced subcellular antioxidant defense in maize plants, J. Integr. Plant Biol., 2008, vol. 50, no. 2, pp. 231–243. https://doi.org/10.1111/j.1744-7909.2007.00594.x

117. Kolbert, Z., Bartha, B., and Erdei, L., Generation of nitric oxide in roots of Pisum sativum, Triticum aestivum and Petroselinum crispum plants under osmotic and drought stress, in Proceedings of the 8th Hungarian Congress on Plant Physiology and the 6th Hungarian Conference on Photosynthesis, Acta Biol. Szeged., 2005, vol. 49, nos. 1–2, pp. 13–16.

118. Tian, X. and Lei, Y., Nitric oxide treatment alleviates drought stress in wheat seedlings, Biol. Plant., 2006, vol. 50, no. 4, pp. 775–778. https://doi.org/10.1007/s10535-006-0129-7

119. Zhang, H., Shen, W.B., and Xu, L.L., Effects of nitric oxide on the germination of wheat seeds and its reactive oxygen species metabolisms under osmotic stress, Acta Bot. Sin., 2003, vol. 45, pp. 901–905.

120. Kolupaev, Yu.E., Karpets, Yu.V., Yastreb, T.O., and Lugovaya, A.A., Combined effect of salicylic acid and nitrogen oxide donor on stress-protective system of wheat plants under drought conditions, Appl. Biochem. Microbiol., 2018, vol. 54, no. 4, pp. 418–424. https://doi.org/10.1134/S0003683818040099

121. Tan, J., Zhao, H., Hong, J., Han, Y., Li, H., and Zhao, W., Effects of exogenous nitric oxide on photosynthesis, antioxidant capacity and proline accumulation in wheat seedlings subjected to osmotic stress, World J. Agricult. Sci., 2008, vol. 4, no. 3, pp. 307–313.

122. Khan, M.N., Mobin, M., Abbas, Z.K., and Siddiqui, M.H., Nitric oxide-induced synthesis of hydrogen sulfide alleviates osmotic stress in wheat seedlings through sustaining antioxidant enzymes, osmolyte accumulation and cysteine homeostasis, Nitric Oxide, 2017, vol. 68, pp. 91–102. https://doi.org/10.1016/j.niox.2017.01.001

123. Shan, C., Zhang, S., and Zhou, Y., Hydrogen sulfide is involved in the regulation of ascorbate–glutathione cycle by exogenous ABA in wheat seedling leaves under osmotic stress, Cereal Res. Commun., 2017, vol. 45, no. 3, pp. 411–420. https://doi.org/10.1556/0806.45.2017.021

124. Jin, Z.P., Shen, J.J., Qiao, Z.J., Yang, G.D., Wang, R., and Pei, Y.X., Hydrogen sulfide improves drought resistance in Arabidopsis thaliana, Biochem. Biophys. Res. Commun., 2011, vol. 414, no. 3, pp. 481–486. https://doi.org/10.1016/j.bbrc.2011.09.090

125. Zhang, H., Ye, Y.K., Wang, S.H., Luo, J.P., Tang, J., and Ma, D., F, Hydrogen sulfide counteracts chlorophyll loss in sweet potato seedling leaves and alleviates oxidative damage against osmotic stress, Plant Growth Regul., 2009, vol. 58, no. 3, pp. 243–250. https://doi.org/10.1007/s10725-009-9372-1

126. Kolupaev, Yu.E., Firsova, E.N., Yastreb, T.O., Ryabchun, N.I., and Kirichenko, V.V., Effect of hydrogen sulfide donor on antioxidant state of wheat plants and their resistance to soil drought, Russ. J. Plant. Physiol., 2019, vol. 66, no. 1, pp. 59–66. https://doi.org/10.1134/S1021443719010084

127. Silva, C.J., Batista, FontesE.P., and Modolo, L.V., Salinity-induced accumulation of endogenous H2S and NO is associated with modulation of the antioxidant and redox defense systems in Nicotiana tabacum L. cv. Havana, Plant Sci., 2017, vol. 256, pp. 148–159. https://doi.org/10.1016/j.plantsci.2016.12.011

128. Hasanuzzaman, M., Hossain, M.A., and Fujita, M., Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings, Plant Biotechnol. Rep., 2011, vol. 5, pp. 353–365. https://doi.org/10.1007/s11816-011-0189-9

129. Ali, Q., Daud, M.K., Haider, M.Z., Ali, S., Rizwan, M., Aslam, N., Noman, A., Iqbal, N., Shahzad, F., Deeba, F., Ali, I., and Zhu, S.J., Seed priming by sodium nitroprusside improves salt tolerance in wheat (Triticum aestivum L.) by enhancing physiological and biochemical parameters, Plant Physiol. Biochem., 2017, vol. 119, pp. 50–58. https://doi.org/10.1016/j.plaphy.2017.08.010

130. Kausar, F. and Shahbaz, M., Interactive effect of foliar application of nitric oxide (NO) and salinity on wheat (Triticum aestivum L.), Pak. J. Bot., 2013, vol. 45, pp. 67–73.

131. Kausar, F. and Shahbaz, M., Ashraf M, Protective role of foliar-applied nitric oxide in Triticum aestivum under saline stress, Turk. J. Bot., 2013, vol. 37, pp. 1155–1165. https://doi.org/10.3906/bot-1301-17

132. Zhang, Y., Wang, L., Liu, Y., Zhang, Q., Wei, Q., and Zhang, W., 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, no. 3, pp. 545–555. https://doi.org/10.1007/s00425-006-0242-z

133. Ahmad, P., Abdel, Latef A.A., Hashem, A., Abd, Allah E.F., Gucel, S., and Tran, L.S., Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front. Plant Sci., 2016, vol. 7, p. 347.

134. Hasanuzzaman, M., Oku, H., Nahar, K.M., Bhuyan, H.M.B., Mahmud, J.A., Baluska, F., and Fujita, M., Nitric oxide-induced salt stress tolerance in plants: ROS metabolism, signaling, and molecular interactions, Plant Biotechnol. Rep., 2018, vol. 12, no. 2, pp. 77–92. https://doi.org/10.1007/s11816-018-0480-0

135. Manai, J., Kalai, T., Gouia, H., and Corpas, F.J., Exogenous nitric oxide (NO) ameliorates salinity-induced oxidative stress in tomato (Solanum lycopersicum) plants, J. Soil Sci. Plant Nutr., 2014, vol. 14, no. 2, pp. 433–446. https://doi.org/10.4067/S0718-95162014005000034

136. Zhao, G., Zhao, Y., Yu, X., Kiprotich, F., Han, H., Guan, R., Wang, R., and Shen, W., Nitric oxide is required for melatonin-enhanced tolerance against salinity stress in rapeseed (Brassica napus L.) seedlings, Int. J. Mol. Sci., 2018, vol. 19, no. 7, p. 1912. https://doi.org/10.3390/ijms19071912

137. Saddhe, A.A., Malvankar, M.R., Karle, S.B., and Kumar, K., Reactive nitrogen species: paradigms of cellular signaling and regulation of salt stress in plants, Environ. Exp. Bot., 2018 (in press). https://doi.org/10.1016/j.envexpbot.2018.11.010

138. Lai, D.W., Mao, Y., Zhou, H., Li, F., Wu, M., Zhang, J., He, Z., Cui, W., and Xie, Y., Endogenous hydrogen sulfide enhances salt tolerance by coupling the reestablishment of redox homeostasis and preventing salt-induced K+ loss in seedlings of Medicago sativa, Plant Sci., 2014, vol. 225, pp. 117–129. https://doi.org/10.1016/j.plantsci.2014.06.006

139. Janicka, M., Reda, M., Czyzewska, K., and Kabala, K., Involvement of signalling molecules NO, H2O2 and H2S in modification of plasma membrane proton pump in cucumber roots subjected to salt or low temperature stress, Funct. Plant Biol., 2017, vol. 45, no. 4, pp. 428–439. https://doi.org/10.1071/FP17095