Фізіологія рослин і генетика 2019, том 51, № 5, 371-387, doi: https://doi.org/10.15407/frg2019.05.371

Нітратредуктаза та її роль у бобово-ризобіальному симбіозі

Коць С.Я., Михалків Л.М.

  • Інститут фізіології рослин і генетики Національної академії наук України 03022 Київ, вул. Васильківська, 31/17

Наведено огляд вітчизняної та зарубіжної літератури, що стосується будови нітратредуктази, її локалізації та функціонування, зокрема у бобово-ризобіальних симбіотичних системах. Висвітлено питання, присвячені регуляції синтезу та активності цього ферменту, показано їх зумовленість чинниками зовнішнього середовища і можливість зниження інгібувальної дії останніх при застосуванні певних прийомів. Зазначено, що в кореневих бульбочках бобових, які формуються в результаті взаємодії рослин і ризобій, відбуваються процеси відновлення нітратного й молекулярного азоту, в яких беруть участь відповідно нітратредуктаза і нітрогеназа. За наявності в симбіозі бобова рослина—бульбочкові бактерії активної системи фіксації атмосферного азоту нітратредуктаза може по-різному взаємодіяти з нітрогеназою залежно від локалізації і типу ферменту, генетичних особливостей симбіонтів, умов культивування бобових. Розглянуто гіпотези щодо можли­вих механізмів взаємодії обох ферментів, наведено дані про розподіл нітра­тредуктазної активності в різних зонах бульбочки. Розкрито роль нітратредуктази в азотному живленні й формуванні урожаю рослин. Окремо висвітлено значення монооксиду азоту для рослин та участі нітратредуктази в його синтезі. Окреслено можливі шляхи оптимізації функціонування нітратредуктази з метою підвищення ефективності симбіозу й продуктивності рослин.

Ключові слова: нітратредуктаза, нітрогеназа, азотне живлення рослин, бобово-ризобіальний симбіоз, бульбочки, нітрати, монооксид азоту, продуктивність

Фізіологія рослин і генетика
2019, том 51, № 5, 371-387

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1. Chamizo-Ampudia, A., Sanz-Luque, E., Llamas, A., Galvan, A. & Fernandes, E. (2017). Nitrate reductase regulates plant nitric oxide homeostasis. Trends Plant Sci., 22, pp. 163-174. https://doi.org/10.1016/j.tplants.2016.12.001

2. Crawford, N.M. & Glass, A.D. (1998). Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci., 3, pp. 389-395. https://doi.org/10.1016/S1360-1385(98)01311-9

3. Broadley, M., Brown, P., Buerkert, A., Cakmak, I., Cooper, J., Eichert, T., Engels, C., Fernandez, V., Kirkby, E. & George, E. (2012). Marschner's mineral nutrition of higher plants. Cambridge: Academic Press.

4. Beatty, P.H., Klein, M.S., Fischer, J.J., Lewis, I.A., Muench, D.G. & Good, A.G. (2016). Understanding plant nitrogen metabolism through metabolomics and computational approaches. Plants-Basel, 5(4), p. 39. https://doi.org/10.3390/plants5040039

5. Xu, G., Fan, X. & Miller, A.J. (2012). Plant nitrogen assimilation and use efficiency. Annu. Rev. Plant Biol., 63, pp. 153-182. https://doi.org/10.1146/annurev-arplant-042811-105532

6. Campbell, W.H. (1999). Nitrate reductase structure, functioning and regulation: bridging and gap between biochemistry and physiology. Annu. Rev. Plant Physiol. Plant Mol. Biol., 50, pp. 277-303. https://doi.org/10.1146/annurev.arplant.50.1.277

7. Tischner, R. (2000). Nitrate uptake and reduction in higher and lower plants. Plant, Cell Environ., 23, pp. 1005-1024. https://doi.org/10.1046/j.1365-3040.2000.00595.x

8. Stцhr, C. & Ullrich, W.R. (2002). Generation and possible roles of NO in plant roots and their apoplastic space. J. Exp. Bot., 53, pp. 2293-2303. https://doi.org/10.1093/jxb/erf110

9. Forde, B.G. (2002). Local and long-range signaling pathways regulating plant responses to nitrate. Annu. Rev. Plant Biol., 53, pp. 203-224. https://doi.org/10.1146/annurev.arplant.53.100301.135256

10. Xiong, J., Fu, G., Yang, Y., Zhu, Ch. & Tao, L. (2012). Tungstate: is it really a specific nitrate reductase inhibitor in plant nitric oxide research? J. Exp. Bot., 63, pp. 33-41. https://doi.org/10.1093/jxb/err268

11. Saroop, S., Thaker, V.S., Chanda, S.V. & Singh, Y.D. (1998). Light and nitrate induction of nitrate reductase in kinetin- and gibberellic acid-treated mustard cotyledons. Acta Physiol. Plant., 20, pp. 359-362. https://doi.org/10.1007/s11738-998-0020-6

12. Arora, V., Ghosh, M.K., Singh, P. & Gangopadhyay, G. (2018). Light regulation of nitrate reductase gene expression and enzyme activity in the leaves of mulberry. Indian J. Biochem. Biophys., 55, pp. 62-66.

13. Tischner, R., Peuke, A., Godbold, D.L., Feig, R., Merg, G. & Huttermann, A. (1988). The effect of NO-fumigation on aseptically grown spruce seedlings. J. Plant Physiol., 133, pp. 243-246. https://doi.org/10.1016/S0176-1617(88)80145-7

14. Hufton, C.A., Besford, R.T. & Wellburn, A.R. (1996). Effects of NO (+ NO2) pollution on growth, nitrate reductase activities and associated protein contents in glasshouse lettuce grown hydroponically in winter with CO2 enrichment. New Phytol., 133, No. 3, pp. 495-501. https://doi.org/10.1111/j.1469-8137.1996.tb01917.x

15. Weber, P., Thoene, B. & Rennenberg, H. (1998). Absorption of atmospheric NO2 by spruce (Picea abies) trees. III. Interaction with nitrate reductase activity in the needles and phloem transport. Bot. Acta, 111, pp. 377-382. https://doi.org/10.1111/j.1438-8677.1998.tb00722.x

16. Foyer, C.H., Valadier, M.H., Migge, A. & Becker, T.W. (1998). Drought-induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves. Plant Physiol., 117, No. 1, pp. 283-292. https://doi.org/10.1104/pp.117.1.283

17. Munjal, N., Sawhney, S.K. & Sawhney, V. (1997). Activation of nitrate reductase in extracts of water stressed wheat. Phytochemistry, 45, pp. 659-665. https://doi.org/10.1016/S0031-9422(97)00058-7

18. Kots, S.Ya., Veselovska, L.I. & Mykhalkiv, L.M. (2014). The nitrate reductase activity in the leaves of soybean inoculated with Bradyrhizobium japonicum under different water supply and lectin application. Nauk. zap. Ternop. nats. ped. un-tu. Ser. Biol., 60, No. 3, pp. 114-117 [in Ukrainian].

19. Mykhalkiv, L.M. (2015). The influence of lectin on nitrogen fixation activity and nitrate reduction in alfalfa plants inoculated with rhizobia under different water supply. Fiziol. rast. genet., 47, No. 5, pp. 440-446 [in Ukrainian].

20. Khan, M.G., Silberbush, M. & Lips, S.H. (1995). Physiological studies on salinity and nitrogen interaction in alfalfa plants: III. Nitrate reductase activity. J. Plant Nutr., 8, No. 11, pp. 2495-2500. https://doi.org/10.1080/01904169509365079

21. Khan, M.G. & Srivastava, H.S. (1998). Changes in growth and nitrogen assimilation in maize plants induced by NaCl and growth regulators. Biol. Plant., 41, pp. 93-99. https://doi.org/10.1023/A:1001768601359

22. Toselli, M., Flore, J.A., Marangoni, B. & Masia, A. (1999). Effects of root-zone temperature on nitrogen accumulation by nonbearing apple trees. J. Hortic. Sci. Biotech., 74, pp. 118-124. https://doi.org/10.1080/14620316.1999.11511083

23. Stoyanov, I., Atanasova, L. & Ginina, D. (1994). Effect of some cytokinins on maize nitrate reductase activity at salinity. Bulg. J. Plant Physiol., 20, pp. 5-10.

24. Wang, Z.Y., Tang, Y.L. & Zhang, F.S. (1999). Effect of molybdenum on growth and nitrate reductase activity of winter wheat seedlings as influenced by temperature and nitrogen treatments. J. Plant Nutr., 1999, 22, pp. 387-395. https://doi.org/10.1080/01904169909365636

25. Kaiser, W.M., Weiner, H. & Huber, S.C. (1999). Nitrate reductase in higher plants: a case study for transduction of environmental stimuli into control of catalytic activity. Physiol. Plant., 105, pp. 385-390. https://doi.org/10.1034/j.1399-3054.1999.105225.x

26. Kaiser, W.M. & Huber, S.C. (2001). Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. J. Exp. Bot., 52, pp. 1981-1989. https://doi.org/10.1093/jexbot/52.363.1981

27. Kots, S.Ya., Morgun, V.V., Patyka, V.F., Datsenko, V.K., Krugova, E.D., Kyrychenko, E.V., Melnykova, N.N. & Mykhalkiv, L.M. (2010). Biological nitrogen fixation. Vol. 1. Kyiv: Logos [in Russian].

28. Silveira, J.A.G., Matos, J.C.S., Cecatto, V.M., Viegas, R.A. & Oliveira, J.T.A. (2001). Nitrate reductase activity, distribution, and response to nitrate in two contrasting Phaseolus species inoculated with Rhizobium spp. Environ. Exp. Bot., 46, pp. 37-46. https://doi.org/10.1016/S0098-8472(01)00082-X

29. Delfini, R., Belgoff, C., Fernandez, E., Fabra, A. & Castro, S. (2010). Symbiotic nitrogen fixation and nitrate reduction in the peanut cultivars with different growth habit and branching pattern structures. Plant Growth Regul., 61, pp. 153-159. https://doi.org/10.1007/s10725-010-9461-1

30. Caba, J.M., Lluch, C., Hervas, A. & Ligero, F. (1990). Nitrate metabolism in roots and nodules of Vicea faba in response to exogenous nitrate. Physiol. Plant., 79, pp. 531-539. https://doi.org/10.1111/j.1399-3054.1990.tb02114.x

31. Becana, M. & Sprent, J. (1987). Nitrogen fixation and nitrate reduction in the root nodules of legumes. Physiol. Plant., 70, pp. 757-765. https://doi.org/10.1111/j.1399-3054.1987.tb04335.x

32. Aparicio-Tejo, P. & Sanchez-Diaz, M. (1982). Nodule and leaf nitrate reductase and nitrogen fixation in Medicago sativa L. under warer stress. Plant Physiol., 69, pp. 479-482. https://doi.org/10.1104/pp.69.2.479

33. Hunter, W.J. (1983). Soybean root and nodule nitrate reductase. Physiol. Plant., 59, pp. 471-475. https://doi.org/10.1111/j.1399-3054.1983.tb04232.x

34. Stephens, B.D. & Neyra, C.A. (1983). Nitrate and nitrite reduction in relation to nitrogenase activity in soybean nodules and Rhizobium japonicum bacteroids. Plant Physiol., 71, pp. 731-735. https://doi.org/10.1104/pp.71.4.731

35. Randall, D.D., Russell, W.J. & Johnson, D.R. (1978). Nodule nitrate reductase as a source of reduced nitrogen in soybean, Glycine max. Physiol. Plant., 44, pp. 325-328. https://doi.org/10.1111/j.1399-3054.1978.tb01631.x

36. Oyhama, T. & Kumazawa, K. (1979). Assimilation and transport of nitrogenous compounds originated from N2 fixation and 15NO3- absorption. Soil Sci. Plant Nutr., 2, pp. 9-19. https://doi.org/10.1080/00380768.1979.10433141

37. Vance, C.P. & Heichel, G. (1981). Nitrate assimilation during vegetative regrowth of alfalfa. Plant Physiol., 68, pp. 1052-1056. doi: https://doi.org/10.1104/pp.68.5.1052

38. Sprent, J.I., Giannakis, C. & Wallace, W. (1987). Transport of nitrate and calcium into legume root nodules. J. Exp. Bot., 38, No. 192, pp. 1121-1128. https://doi.org/10.1093/jxb/38.7.1121

39. Giannakis, C., Nicholas, D.J.D. & Wallace, W. (1988). Utilization of nitrate by bacteroids of Bradyrhizobium japonicum in the soybean root nodule. Planta, 174, pp. 51-58. https://doi.org/10.1007/BF00394873

40. Chechetka, S.A., Piskorskaya, V.P., Bruskova, R.K., Troitskaya, G.N. & Izmailov, S.F. (1998). Partitioning of 14C-photoassimilates in soybean plants assimilating of symbiotic and nitrate nitrogen. Fiziologiya rasteniy, 45, No. 2, pp. 241-247 [in Russian].

41. Becana, M., Minchin, F.R. & Sprent, J.I. (1989). Short-term inhibition of legume N2 fixation by nitrate. Nitrate effects on nitrate reductase activities of bacteroids and nodule cytosol. Planta, 180, pp. 40-45. https://doi.org/10.1007/BF02411409

42. Lvov, N.P., Burihanov, Sh.S. & Kretovich, B.L. (1980). The relationship of nitrogenase and nitrate reductase in nitrogen-fixing cells. Prikladnaya biohimiya i mikrobiologiya, XVI(6), pp. 805 [in Russian].

43. Dubrovo, P.N., Ilyasova, V.B., Shirinskaya, M.G., & Yagodin, B.A. (1979). Nitrogen fixing activity of lupine nodules and the content of pyridine nucleotides in them. Fiziologiya rasteniy, 26, No. 3, pp. 599-605 [in Russian].

44. Noel, K.D., Carneol, M. & Brill, W.J. (1982). Nodule protein synthesis and nitrogenase activity of soybeans exposed to fixed nitrogen. Plant Physiol., 70, pp. 1236-1241. https://doi.org/10.1104/pp.70.5.1236

45. Silsbury, J.H., Catchpoole, D.W. & Wallace, W. (1986). Effect of nitrate and ammonium on nitrogenase (C2H2-reduction) activity of swards of subterranean clover Trifolium subterraneum L. Austral. J. Plant Physiol., 13, pp. 257-273. https://doi.org/10.1071/PP9860257

46. Yadav, V.K., Prakash, S. & Kapoor, H.C. (1987). Interaction between nitrate and nitrogen fixation and possible role of indole acetic acid in its regulation in bengal gram (Cicer arietinum) root nodules. Indian J. Exp. Biol., 25, pp. 385-388.

47. Carrol, B.J. & Gresshoff, P.M. (1983). Nitrate inhibition of nodulation and nitrogen fixation in white clower. Z. Pflanzenphysiol, 110, pp. 77-88. https://doi.org/10.1016/S0044-328X(83)80218-9

48. Tatarova, N.K., Lvov, N.P. & Shugaev, N.I. (1976). On the ratio of nitrogenase and nitrate reductase in the cell of nitrobacter. Izv. Timiryazev. s.-h. akad., 3. pp. 24-29 [in Russian].

49. Lvov, N.P. (1989). Molybdenum in the nitrogen assimilation in plants and microorganisms: 43-e Bakhovskoe chtenie. Moscov: Nauka [in Russian].

50. Lvov, N.P., Zabolotnyy, A.I. & Savchenkova, L.M. (1987). Effect and aftereffect of molybdenum on yellow lupine: physiological and biochemical substantiation. Agrohimiya, 11, pp. 89-97 [in Russian].

51. Vahaniya, N.A., Abashidze, N.D. & Nutsubidze, N.N. (1987). Short-term effect of nitrate and molybdate on nitrogenase activity and nitrate assimilation in the bacteroid of bean nodules. Fiziologiya i biohimiya kult. rasteniy, 19, No. 3, pp. 220-226 [in Russian].

52. Fedorova, E.E. & Patatuyeva, Yu.A. (1984). Ultrastructure and nitrogen-fixing activity of red clover nodules under molybdenum application. Fiziologiya rasteniy, 31, No. 6, pp. 1121-1126 [in Russian].

53. Lucinski, R., Polcyn, W. & Ratajczak, L. (2002). Nitrate reduction and nitrogen fixation in symbiotic association Rhizobium-legumes. Acta Biochim. Pol., 49, No. 2, pp. 537-546.

54. Layzell, D.B. & Hunt, S. (1990). Oxygen and the regulation of nitrogen fixation in legume nodule. Physiol. Plant., 80, pp. 322-327. https://doi.org/10.1111/j.1399-3054.1990.tb04414.x

55. Ianetta, P.P.M., de Lorenzo, C., James, E.K., Fernбndez-Pascual, M., Sprent, J.I., Lucas, M.M., Witty, J.F., de Felipr, M.R. & Minchin, F.R. (1993). Oxygen diffusion in lupine nodules. I. Visualisation of diffusion barrier operation. J. Exp. Bot., 44, No. 26, pp. 1461-1467. https://doi.org/10.1093/jxb/44.9.1461

56. Minchin, F.R. (1997). Regulation of oxygen diffusion in legume nodules. Soil Biol. Biochem., 29, pp. 881-888. https://doi.org/10.1016/S0038-0717(96)00204-0

57. Becana, M. & Klucas, R.V. (1992). Oxidation and reduction of leghemoglobin in root nodules of leguminous plants. Plant Physiol., 98, pp. 1217-1221. https://doi.org/10.1104/pp.98.4.1217

58. Parsons, R. & Day, D.A. (1990). Mechanisms of soybean nodule adaptation to different oxygen pressures. Plant Cell Environ., 13, pp. 501-512. https://doi.org/10.1111/j.1365-3040.1990.tb01066.x

59. Chamber-Perez, M.A., Camacho-Martinez, M. & Soriano-Niebla, J. (1997). Nitrate-reductase activities of Bradyrhizobium spp. in tropical legumes: Effects of nitrate on O2 diffusion in nodules and carbon costs of N2 fixation. Plant Physiol., 150, pp. 92-96. https://doi.org/10.1016/S0176-1617(97)80186-1

60. Serrano, A. & Chamber, M. (1990). Nitrate reduction in Bradyrhizobium sp. (Lupinus) strains and its effect on their symbiosis with Lupinus luteus. J. Plant Physiol., 136, pp. 240-246. https://doi.org/10.1016/S0176-1617(11)81673-1

61. Sidorova, K.K., Godovikova, V.A. & Stolyarova, S.N. (1988). Investigation of nitrogenase and nitrate reductase activity in pea mutants. Genetika, 24, No. 1, pp. 136-140 [in Russian].

62. Arrese-Igor, C., Garcia-Plazaola, J.I., Hernandez, A. & Aparicio-Tejao, P.M. (1990). Effect of low nitrate supply to nodulated lucerne on time course of activities of enzymes involved in inorganic nitrogen metabolism. Physiol. Plant., 80, pp. 185-190. https://doi.org/10.1111/j.1399-3054.1990.tb04394.x

63. Arrese-Igor, C., Minchin, F.R., Gordon, A.J. & Nath, A.K. (1997). Possible causes of the physiological decline in soybean nitrogen fixation in the presence of nitrate. J. Exp. Bot., 48, pp. 905-913. doi: https://doi.org/10.1093/jxb/48.4.905

64. Cheniae, G. & Evans, H.J. (1960). Physiological studies on nodule-nitrate reductase. Plant Physiol., 35, pp. 454-462. https://doi.org/10.1104/pp.35.4.454

65. Kondorosi, A., Barabas, T., Svab, Z., Orosz, L., Sik, T. & Hotchkiss, R.D. (1973). Evidence for common genetic determinants of nitrogenase andnitrate reductase in Rhizobium meliloti. Nat. New Biol., 246, pp. 153-154. https://doi.org/10.1038/newbio246153a0

66. Streeter, J.G. & Devine, P.J. (1983). Evaluation of nitrate reductase activity in Rhizobium japonicum. Appl. Environ. Microbiol., 46, pp. 521-524.

67. Pagan, J.D., Scowcroft, W.R., Dudman, W.F. & Gibson, A.H. (1977). Nitrogen fixation in nitrate reductase-deficient mutantas of cultured rhizobia. J. Bacteriol., 129, No. 2, pp. 718-723.

68. Antoun, H., Bordeleau, L.M., Prevost, D. & Lachance, R.A. (1980). Absence of a correlation between nitrate reductase and symbiotic nitrogen fixation efficiency in Rhizobium meliloti. Can. J. Plant Sci., 60, No. 1, pp. 209-212. https://doi.org/10.4141/cjps80-028

69. Cookson, S.J., Williams, L.E. & Miller, A.J. (2005). Light-dark changes in cytosolic nitrate pools depend on nitrate reductase activity in Arabidopsis leaf cells. Plant Physiol., 138, pp. 1097-1105. https://doi.org/10.1104/pp.105.062349

70. Miller, A.J. & Smith, S.J. (2008). Cytosolic nitrate ion homeostasis: Could it have a role in sensing nitrogen status? Ann. Bot., 101, pp. 485-489. https://doi.org/10.1093/aob/mcm313

71. Fan, X., Gordon-Weeks, R., Shen, Q. & Miller, A.J. (2006). Glutamine transport and feedback regulation of nitrate reductase activity in barley roots leads to changes in cytosolic nitrate pools. J. Exp. Bot., 57, No. 6, pp. 1333-1340. https://doi.org/10.1093/jxb/erj110

72. Miller, A.J., Fan, X., Orsel, M., Smith, S.J. & Wells, D.M. (2007). Nitrate transport and signalling. J. Exp. Bot., 58, pp. 2297-2306. doi: https://doi.org/10.1093/jxb/

73. Fany, A., Foyer, C.H. & Gupta, K.J. (2018). Nitrate, NO and ROS signaling in stem cell homeostasis. Trends Plant Sci., 23, pp. 1041-1044. https://doi.org/10.1016/j.tplants.2018.09.010

74. Izmailov, S.F., Nikitin, A.V. & Rodionov, V.A. (2018). Nitrate signaling in plants: introduction to the problem. Russ. J. Plant Physiol., 65, pp. 477-489. https://doi.org/10.1134/S1021443718040027

75. Wang, R., Okamoto, M., Xing, X. & Crawford, N.M. (2003). Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol., 132, pp. 556-567. https://doi.org/10.1104/pp.103.021253

76. Salgado, I., Martinez, M.C., Oliveira, H.C. & Frungillo, L. (2013). Nitric oxide signaling and homeostasis in plants: a focus on nitrate reductase and S-nitrosoglutatione reductase in stress-related responses. Braz. J. Bot., 36, pp. 89-98. https://doi.org/10.1007/s40415-013-0013-6

77. Besson-Bard, A., Pugin, A. & Wendehenne, D. (2008). New insights into nitric oxide signaling in plants. Annu Rev. Plant Biol., 59, pp. 21-39. https://doi.org/10.1146/annurev.arplant.59.032607.092830

78. Corpas, F.J., Palma, J.M., del Rio, L.A. & Barroso, J.B. (2009). Evidence supporting the existence of L-arginine-dependent nitric oxide synthase activity in plants. New Phytol., 184, pp. 9-14. https://doi.org/10.1111/j.1469-8137.2009.02989.x

79. Moreau, M., Lindermayr, C., Durner, J. & Klessig, D.F. (2010). NO synthesis and signaling in plants: where do we stand? Physiol. Plant., 138, pp. 372-383. https://doi.org/10.1111/j.1399-3054.2009.01308.x

80. Delledonne, M., Xia, Y., Dixon, R.A. & Lamb, C. (1998). Nitric oxide functions as a signal in plant disease resistance. Nature, 394, pp. 585-588. https://doi.org/10.1038/29087

81. Durner, J., Wendehenne, D. & Klessig, D.F. (1998). Defence gene induction in tobacco by nitric oxide, cyclic GMP and cyclic ADP-ribose. PNAS USA, 95, pp. 10328-10333. https://doi.org/10.1073/pnas.95.17.10328

82. Durner, J. & Klessing, D. (1999). Nitric oxide as a signal in plants. Curr. Opin. Plant Biol., 2, pp. 369-374. https://doi.org/10.1016/S1369-5266(99)00007-2

83. Grawford, N.M. & Guo, F.Q. (2005). New insights into nitric oxide metabolism and regulatory function. Trends Plant Sci., 10, pp. 195-200. https://doi.org/10.1016/j.tplants.2005.02.008

84. Wilson, I.D., Neill, S.J. & Hancock, J.T. (2008). Nitric oxide synthesis and signaling in plant. Plant Cell Environ., 31, pp. 622-631. https://doi.org/10.1111/j.1365-3040.2007.01761.x

85. Wendehenne, D. & Hancock, J.T. (2011). New frontiers in nitric oxide biology in plant. Plant Sci., 181, No. 5, pp. 507-508. https://doi.org/10.1016/j.plantsci.2011.07.010

86. Corpas, F.J., Leterrier, M., Valderrama, R., Airaki, M., Chaki, M., Palma, J.M. & Barroso, J.B. (2011). Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci, 181, No. 5, pp. 604-611. https://doi.org/10.1016/j.plantsci.2011.04.005

87. Mur, L.A., 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, pp. 215. https://doi.org/10.3389/fpls.2013.00215

88. Santolini, J., Andre, F., Jeandroz, S. & Wendehenne, D. (2017). Nitric oxide synthase in plants: Where do we stand? Nitric Oxide, 63, pp. 30-38. https://doi.org/10.1016/j.niox.2016.09.005

89. Astier, J., Gross, I. & Durner, J. (2018). Nitric oxide production in plants: An update. J. Exp. Bot., 69, pp. 3401-3411. https://doi.org/10.1093/jxb/erx420

90. Shimoda, Y., Nagata, M., Suzuki, A., Abe, M., Sato, S., Kato, T., Tabata, S., Higashi, S. & Uchiumi, T. (2005). Symbiotic rhizobium and nitric oxide induce gene expression of non-symbiotic hemoglobin in Lotus japonicus. Plant Cell Physiol., 46, pp. 99-107. https://doi.org/10.1093/pci/pci001

91. Nagata, M., Murakami, E., Shimoda, Y., Shimoda-Sasakura, F., Kucho, K., Suzuki, A., Abe, M., Higashi, S. & Uchiumi, T. (2008). Expression of a class 1 hemoglobin gene and production of nitric oxide in response to symbiotic and pathogenic bacteria in Lotus japonicus. Mol. Plant-Microbe Interact., 21, No. 9, pp. 1175-1183. https://doi.org/10.1094/MPMI-21-9-1175

92. Pii, Y., Crimi, M., Cremonese, G., Spena, A. & Pandolfini, T. (2007). Auxin and nitric oxide control indeterminate nodule formation. BMC Plant Biol., 7, p. 21. https://doi.org/10.1186/1471-2229-7-21

93. Baudouin, E., Pieuchot, L., Engler, G., Pauly, N. & Puppo, A. (2006). Nitric oxide is formed in Medicago truncatula-Sinorhizobium meliloti functional nodules. Mol. Plant-Microbe Interact., 19, No. 9, pp. 970-975. https://doi.org/10.1094/MPMI-19-0970

94. Meakin, G.E., Bueno, E., Jepson, B., Bedmar, E.J., Richardson, D.J. & Delgado, M.J. (2007). The contribution of bacteroidal nitrate and nitrite reduction to the formation of nitrosyl leghaemoglobin complexes in soybean root nodules. Microbiology, 153, pp. 411-419. https://doi.org/10.1099/mic.0.2006/000059-0

95. Sanchez, C., Gates, A.J., Meakin, G.E., Uchiumi, T., Girard, L., Richardson, D.J., Bedmar, E.J. & Delgado, M.J. (2010). Production of nitric oxide and nitrosylleghemoglobin complexes in soybean nodules in response to flooding. Mol. Plant-Microbe Interact., 23, No. 5, pp. 702-711. https://doi.org/10.1094/MPMI-23-5-0702

96. Ferrarini, A., de Stefano, M., Baudouin, E., Pucciariello, C., Polverari, A., Puppo, A. & Delledonne, M. (2008). Expression of Medicago truncatula genes responsive to nitric oxide in pathogenic and symbiotic conditions. Mol. Plant-Microbe Interact., 21, No. 6, pp. 781-790. https://doi.org/10.1094/MPMI-21-6-0781

97. Herold, S. & Puppo, A. (2005). Oxyleghemoglobin scavenges nitrogen monoxide and peroxynitrite: a possible role in functioning nodules? J. Biol. Inorg. Chem., 10, No. 8, pp. 935-945. https://doi.org/10.1007/s00775-005-0046-9

98. Trinchant, J.C. & Rigaud, J. (1982). Nitrite and nitric oxide as inhibitors of nitrogenase from soybean bacteroids. Appl. Environ. Microbiol., 44, No. 6, pp. 1385-1388.

99. Shimoda, Y., Shimoda-Sasakura, F., Kucho, K., Kanamori, N., Nagata, M., Suzuki, A., Abe, M., Higashi, S. & Uchiumi, T. (2009). Overexpression of class 1 plant hemoglobin genes enhances symbiotic nitrogen fixation activity between Mesorhizobium loti and Lotus japonicus. Plant J., 57, pp. 254-263. https://doi.org/10.1111/j.1365-313X.2008.03689.x

100. Kato, K., Kanahama, K. & Kanayama, Y. (2010). Involvement of nitric oxide in the inhibition of nitrogenase activity by nitrate in Lotus root nodules. J. Plant Physiol., 167, pp. 238-241. https://doi.org/10.1016/j.jplph.2009.08.006

101. Meilhoc, E., Cam, Y., Skapski, A. & Bruand, C. (2010). The response to nitric oxide of the nitrogen-fixing symbiont Sinorhizobium meliloti. Mol. Plant-Microbe Interact., 23, No. 6, pp. 748-759. https://doi.org/10.1094/MPMI-23-6-0748

102. Puppo, A., Pauly, N., Boscari, A., Mandon, K. & Brouquisse, R. (2013). Hydrogen peroxide and nitric oxide: key regulators of the Legume-Rhizobium and mycorrhizal symbioses. Antioxid. Redox Signal., 18, No. 16, pp. 2202-2219. https://doi.org/10.1089/ars.2012.5136

103. Boscari, A., Meilhoc, E., Castella, C., Bruand, C., Puppo, A. & Brouquisse, R. (2013). Which role for nitric oxide in symbiotic N2-fixing nodules: toxic by-product or useful signaling/metabolic intermediate? Front. Plant Sci., 4, p. 384. https://doi.org/10.3389/fpls.2013.00384

104. Hichri, I., Boscari, A., Castella, C., Rovere, M., Puppo, A. & Brouquisse, R. (2015). Nitric oxide: a multifaceted regulator of the nitrogen-fixing symbiosis. J. Exp. Bot., 66, pp. 2877-2887. https://doi.org/10.1093/jxb/erv051

105. de Bruij, F.J. (Ed.). (2015). Biological nitrogen fixation. New York: John Wiley & Sons, Inc. https://doi.org/10.1002/9781119053095.ch64

106. Zumft, W.G. (1997). Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev., 61, pp. 533-616.

107. Damiani, I., Pauly, N., Puppo, A., Brouquisse, R. & Boscari, A. (2016). Reactive oxygen species and nitric oxide control early steps of the Legume-Rhizobium symbiotic interaction. Front. Plant Sci., 7, pp. 454. https://doi.org/10.3389/fpls.2016.00454

108. Horchani, F., Prevot, M., Boscari, A., Evangelisti, E., Meilhoc, E., Bruand, C., Raymond, Ph., Boncompagni, E., Aschi-Smiti, S., Puppo, A. & Brouquisse, R. (2011). Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiol., 155, pp. 1023-1036. https://doi.org/10.1104/pp.110.166140

109. Tejada-Jimenez, M., Llamas, A., Galvan, A. & Fernandez, E. (2019). Role of nitrate reductase in NO production in photosynthetic eucaryotes. Plants, 8, p. 56. https://doi.org/10.3390/plants8030056

110. Glyan'ko, A.K. & Mitanova, N.B. (2008). Physiological mechanisms of negative influence of high dozes of mineral nitrogen on legume-rhizobial symbiosis. Visnyk HNAU. Seriya Biologiya, 2, pp. 26-41 [in Russian].

111. Caba, M., Lluch, C. & Ligero, F. (1994). Genotypic variability of nitrogen metabolism enzymes in nodulated roots of Vicia faba. Soil Biol. Biochem., 26, pp. 785-789. https://doi.org/10.1016/0038-0717(94)90274-7

112. Hervas, A., Ligero, F. & Lluch, C. (1991). Nitrate reduction in pea plants: effects of nitrate application and Rhizobium strains. Soil Biol. Biochem., 23, pp. 695-699. https://doi.org/10.1016/0038-0717(91)90085-X

113. Harper, J.E. & Gibson, A.H. (1984). Differential nodulation tolerance to nitrate among legume species. Crop Sci., 24, No. 4, pp. 797-801. https://doi.org/10.2135/cropsci1984.0011183X002400040040x