Fiziol. rast. genet. 2019, vol. 51, no. 1, 3-27, doi:

Phytohormonal regulation of legume-rhizobium symbiosis

Kots S.Ya., Gryshchuk O.O.

  • Institute of Plant Physiology and Genetics, National Academy of Sciences of Ukraine  31/17 Vasylkivska St., Kyiv, 03022, Ukraine

The review devoted to analysis of the literature data concerning main signaling pathways of the nodulation process regulation. The mechanisms of the positive regulation of nodulation mediated by cytokinins, auxins, gibberellins, strigolactones, and of the negative regulation mediated by ethylene, abscisic acid, jasmonic acid, and salicylic acid are thoroughly summarized and discussed. Negative regulation of nodulation processes consists in systemic autoregulation and local hormonal regulation resulting in the change of nodules number. The role of cytokinin family phytohormones in the systemic autoregulation of the nodulation process is also described. Coordination of hormonal signaling pathways is essential process for the root nodule organogenesis, and is a complex of reactions and processes. The concentrations of hormones and other signal components are critical and their decreasing or increasing can lead to the interruption of nodulation. Understanding of the mechanisms of the regulation of nodule formation processes will support the solving of global biotechnological problems and improve agriculture production of legumes.

Keywords: phytohormones, Nod factors, legume-rhizobium symbiosis, nodulation, nitrogen fixation, signaling, autoregulation of nodulation

Fiziol. rast. genet.
2019, vol. 51, no. 1, 3-27

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1. Murray, J.D. (2011). Invasion by invitation: rhizobial infection in legumes. Mol. Plant-Microbe Interact., 24, No. 6, pp. 631-639.

2. Reid, D.E., Ferguson, B.J., Hayashi, S., Lin, Y.H. & Gresshoff, P.M. (2011). Molecular mechanisms controlling legume autoregulation of nodulation. Ann. Bot., 108, pp. 789-795.

3. Held, M., Bonfante, P., Stougaard, J. & Szczyglowski, K. (2010). Common and not so common symbiotic entry. Trends Plant Sci., 15, pp. 540-545.

4. Desbrosses, G.J. & Stougaard, J. (2011). Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe, 10, No. 4, pp. 348-358.

5. Oldroyd, G.E. & Downie, J.A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol., 59, pp. 519-546.

6. Madsen, L.H., Tirichine, L., Jurkiewicz, A., Sullivan, J.T., Heckmann, A.B., Bek, A.S., Ronson, C.W., James, E.K. & Stougaard, J. (2010). The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat. Commun., 1, No. 10, pp. 1-12.

7. Redmond, J.W., Batley, M., Djordjevic, M.A., Innes, R.W., Kuempel, P.L. & Rolfe, B.G. (1986). Flavones induce expression of nodulation genes in Rhizobium. Nature, 323, pp. 632-635.

8. Pueppke, S.G. & Broughton, W.J. (1999). Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol. Plant-Microbe Interact., 12, pp. 293-318.

9. Denarie, J., Debelle, F. & Prome, J.C. (1996). Rhizobium lipochitooligosaccharide nodulation factors: Signalling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem., 65, pp. 503-535.

10. Giraud, E., Moulin, L., Vallenet, D., Barbe, V., Cytryn, E., Avarre, J.C., Jaubert, M., Simon, D., Cartieaux, F., Prin, Y., Bena, G., Hannibal, L., Fardoux, J., Kojadinovic, M., Vuillet, L., Lajus, A., Cruveiller, S., Rouy, Z., Mangenot, S., Segurens, B., Dossat, C., Franck, W.L., Chang, W.S., Saunders, E., Bruce, D., Richardson, P., Normand, P., Dreyfus, B., Pignol, D., Stacey, G., Emerich, D., Vermeglio, A., Medigue, C. & Sadowsky, M. (2007). Legumes symbioses: absence of Nod Genes in photosynthetic bradyrhizobia. Science, 316, pp. 1307-1312.

11. Gough, C. & Cullimore, J. (2011). Lipochitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol. Plant-Microbe Interact., 24, pp. 867-878.

12. Arrighi, J.F., Bersoult, A., Soriano, L.C., Mirabella, R., de Carvalho-Niebel, F., Journet, E.P., Gherardi, M., Huguet, T., Geurts, R., Denarie, J., Rouge, P. & Gough, C. (2006). The Medicago truncatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol., 142, pp. 265-279.

13. Indrasumunar, A., Kereszt, A., Searle, I., Miyagi, M., Li, D., Nguyen, C.D., Men, A., Carroll, B.J. & Gresshoff, P.M. (2009). Inactivation of duplicated Nod-Factor Receptor 5 (NFR5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (Glycine max L. Merr.). Plant Cell Physiol., 51, No. 2, pp. 201-214.

14. Radutoiu, S., Madsen, L.H., Madsen, E.B., Felle, H.H., Umehara, Y., Grшnlund, M., Sato, S., Nakamura, Y., Tabata, S., Sandal, N. & Stougaard, J. (2003). Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature, 425, pp. 585-592.

15. Ke, D., Fang, Q., Chen, C., Zhu, H., Chen, T., Chang, X., Yuan, S., Kang, H., Ma, L., Hong, Z. & Zhang, Z. (2012). The small GTPase ROP6 interacts with NFR5 and is involved in nodule formation in Lotus japonicus. Plant Physiol., 159, No. 1, pp. 131-143.

16. Gough, C. (2003). Rhizobium symbiosis: Insight into nod factor receptors. Curr. Biol., 13, pp. R973-R975.

17. Broghammer, A., Krusell, L., Blaise, M., Sauer, J., Sullivan, J.T., Maolanon, N., Vinther, M., Lorentzen, A., Madsen, E.B., Jensen, K.J., Roepstorff, P., Thirup, S., Ronson, C.W., Thygesen, M.B. & Stougaard, J. (2012). Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc. Natl. Acad. Sci. USA, 109, No. 34, pp. 13859-13864.

18. Huse, M. & Kuriyan, J. (2002). The conformational plasticity of protein kinases. Cell, 109, pp. 275-282.

19. Mitra, R.M., Gleason, C.A., Edwards, A., Hadfield, J., Downie, J.A., Oldroyd, G.E. & Long, S.R. (2004). A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc. Natl. Acad. Sci. USA, 101, pp. 4701-4705.

20. Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneko, T., Tabata, S., Sandal, N., Stougaard, J., Szczyglowski, K. & Parniske, M. (2002). A plant receptor-like kinase required for both fungal and bacterial symbiosis. Nature, 417, pp. 959-962.

21. Limpens, E., Franken, C., Franssen, H., Bisseling, T. & Geurts, R. (2005). Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc. Natl. Acad. Sci. USA, 102, pp. 10375-10380.

22. Glyan'ko, A.K. (2014). Significance of rhizobium nod factors in induction of signaling systems at formation of legume-rhizobia symbiosis. Visn. Kharkivskoho natsionalnoho ahrarnoho un-tu: Seriia Biolohiia, IS. 3, pp. 6-14 [in Russian].

23. Ryu, H., Cho, H., Choi, D. & Hwang, I. (2012). Plant hormonal regulation of nitrogen-fixing nodule organogenesis. Mol. Cells, 34, No. 2, pp. 117-26.

24. Ane, J.M., Kiss, G.B., Riely, B.K., Penmetsa, R.V., Oldroyd, G.E., Ayax, C., Levy, J., Debelle, F., Baek, J.M., Kalo, P., Rosenberg, C., Roe, B.A., Long, S.R., Denarie, J. & Cook, D.R. (2004). Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science, 303, pp. 1364-1367.

25. Gleason, C., Chaudhuri, S., Yang, T., Munoz, A., Poovaiah, B.W. & Oldroyd, G.E. (2006). Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature, 441, pp. 1149-1152.

26. Levy, J., Bres, C., Geurts, R., Chalhoub, B., Kulikova, O., Duc, G., Journet, E.P., Ane, J.M., Lauber, E., Bisseling, T., Denarie, J., Rosenberg, C. & Debelle, F. (2004). A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science, 303, pp. 1361-1364.

27. Heckmann, A.B., Lombardo, F., Miwa, H., Perry, J.A., Bunnewell, S., Parniske, M., Wang, T.L. & Downie, J.A. (2006). Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol., 142, pp. 1739-1750.

28. Smit, P., Raedts, J., Portyanko, V., Debelle, F., Gough, C., Bisseling, T. & Geurts, R. (2005). NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science, 308, pp. 1789-1791.

29. Hirsch, S., Kim, J., Munoz, A., Heckmann, A.B., Downie, J.A. & Oldroyd, G.E. (2009). GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell, 21, pp. 545-557.

30. Tirichine, L., Sandal, N., Madsen, L.H., Radutoiu, S., Albrektsen, A.S., Sato, S., Asamizu, E., Tabata, S. & Stougaard, J. (2007). A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science, 315, No. 5808, pp. 104-107.

31. Ferguson, B.J., Indrasumunar, A., Hayashi, S., Lin, M.H., Lin, Y.H., Reid, D.E. & Gresshoff, P.M. (2010). Molecular analysis of legume nodule development and autoregulation. J. Integr. Plant Biol., 52, No. 1, pp. 61-76.

32. Gage, D.J. (2004). Infection and invasion of roots by symbiotic, nitrogenfixing rhizobia during nodulation of temperate legumes. Microbiol. Mol. Biol. Rev., 68, pp. 280-300.

33. Stougaard, J. (2000). Regulators and regulation of legume root nodule development. Plant Physiol., 124, No. 2, pp. 531-540.

34. Makarova, L. Ye. Physiological role of phenolic compounds in the formation of legume-rhizobium symbiosis at pre-infection stage. Visn. Kharkivskoho natsionalnoho ahrarnoho un-tu: Seriia Biolohiia, Is. 2, pp. 25-40 [in Russian].

35. Kots, S.Ya., Morgun, V.V., Patyka, V.P., Melnykova, N.M. & Mamenko, P.M. (2011). Biological nitrogen fixation: genetics of nitrogen fixation, genetic engineering of strains. Vol. 3. Kyiv: Logos, 404 p. [in Russian].

36. Fauvart, M. & Michiels, J. (2008). Rhizobial secreted proteins as determinants of host specificity rhizobium-legume symbiosis. FEMS Microbiol. Lett., 285, No. 1, pp. 1-9.

37. Kots, S.Ya., Morgun, V.V., Patyka, V.P., Malichenko, S.M., Mamenko, P.M., Kiriziy, D.A., Mykhalkiv, L.M., Beregovenko, S.K. & Melnykova, N.M. (2011). Biological nitrogen fixation: legume-rhizobium symbiosis. Vol. 2. Kyiv: Logos [in Russian].

38. Liu, H., Zhang, C., Yang, J., Yu, N. & Wang, E. (2018). Hormone modulation of legume-rhizobial symbiosis. J. Integr. Plant Biol., 60, No. 8, pp. 632-648.

39. Ferguson, B.J. & Mathesius, U. (2014). Phytohormone regulation of legume-rhizobia interactions. J. Chem. Ecol., 40, pp. 770-790.

40. Gamas, P., Brault, M., Jardinaud, M.F. & Frugier, F. (2017). Cytokinins in Symbiotic Nodulation: When, Where, What For? Trends Plant Sci., 22, No. 9, pp. 792-802.

41. Miri, M., Janakirama, P., Held, M., Ross, L. & Szczyglowski, K. (2016). Into the Root: How Cytokinin Controls Rhizobial Infection. Trends Plant Sci., 21, No. 3, pp. 178-186.

42. Cooper, J.B. & Long, S.R. (1994). Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell, 6, pp. 215-225.

43. Kisiala, A., Laffont, C., Emery, R.J. & Frugier, F. (2013). Bioactive cytokinins are selectively secreted by Sinorhizobium meliloti nodulating and nonnodulating strains. Mol. Plant-Microbe Interact., 26, pp. 1225-1231.

44. Ferguson, B.J. & Mathesius, U. (2003). Signaling interactions during nodule development. J. Plant Growth Reg., 22, No. 1, pp. 47-72.

45. Heckmann, A.B.B., Sandal, N., Bek, A.S., Madsen, L.H., Jurkiewicz, A., Nielsen, M.W., Tirichine, L. & Stougaard, J. (2011). Cytokinin induction of root nodule primordia in Lotus japonicus is regulated by a mechanism operating in the root cortex. Mol. Plant-Microbe Interact., 24, pp. 1385-1395.

46. Gryshchuk, O.O., Volkogon, M.V. & Kots, S.Ya. (2011). Ability of strains and Tn5-mutants of Bradyrhizobium japonicum of various efficiency to synthesize phytophormones in vitro. Silskohospodarska mikrobiolohiia: zdobutky ta perspektyvy. Zb. nauk. prats. Chernihiv: TsNITI, pp. 168-173 [in Ukrainian].

47. Gryshchuk, O.O. & Kots, S.Ya. (2013). Ability of strains and Tn5-mutants of Bradyrhizobium japonicum to zeatin and gibberellins synthesis in vitro. Fiziologiya i biohimiya kult. rasteniy, 45, No. 2, pp. 148-154 [in Ukrainian].

48. Gryshchuk, O.O., Gryshchuk, V.S. & Kots, S.Ya. (2014). Effect of symbiotic characteristics of Bradyrhizobium japonicum on cytokinin status of soybean plants. Naukovi zapysky TNPU imeni Volodymyra Hnatiuka. Seriia: biolohiia, No. 3 (60), pp. 65-68 [in Ukrainian].

49. Volkogon, M.V., Mamenko, P.M. & Kots, S.Ya. (2009). IAA and zeatin balance in soybean plants under seeds inoculation with various strains and mutants of Bradyrhizobium japonicum. Fiziologiya i biokhimiya kult. rasteniy, 41, No. 5, pp. 408-415 [in Ukrainian].

50. Plet, J., Wasson, A., Ariel, F., Le Signor, C., Baker, D., Mathesius, U., Crespi, M. & Frugier, F. (2011). MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula. Plant J., 65, pp. 622-633.

51. Murray, J.D., Karas, B.J., Sato, S., Tabata, S., Amyot, L. & Szczyglowski, K. (2007). A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science, 315, No. 5808, pp. 101-104.

52. Held, M., Hou, H., Miri, M., Huynh, C., Ross, L., Hossain, M.S., Sato, S., Tabata, S., Perry, J., Wang, T.L. & Szczyglowski, K. (2014). Lotus japonicus cytokinin receptors work partially redundantly to mediate nodule formation. Plant Cell, 26, No. 2, pp. 678-694.

53. Tsyiganov, V.E. (2018). Molecular genetic and cellular mechanisms of differentiation of symbiotic nodule. Dis. … doktora nauk. SPb, 509 p. [in Russian].

54. Nagata, M. & Suzuki, A. (2014). Effects of phytohormones on nodulation and nitrogen fixation in leguminous plants. Advances in biology and ecology of nitrogen fixation/Ed. T. Ohyama. InTech, pp. 111-128.

55. Mulder, L., Hogg, B., Bersoult, A. & Cullimore, J.V. (2005). Integration of signalling pathways in the establishment of the legume-rhizobia symbiosis. Physiol. Plant, 123, No. 2, pp. 207-218.

56. Hirsch, A., Bhuvaneswari, T., Torrey, J. & Bisseling, T. (1989). Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc. Natl. Acad. Sci. USA, 86, pp. 1244-1248.

57. Wu, C.F., Dickstein, R., Cary, A.J. & Norris, J.H. (1996). The auxin transport inhibitor N-(1-naphthyl)phthalamic acid elicits pseudonodules on nonnodulating mutants of white sweetclover. Plant Physiol., 110, pp. 501-510.

58. Mathesius, U., Schlaman, H.R.M., Spaink, H.P., Sautter, C., Rolfe, B.G. & Djordjevic, M.A. (1998). Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J., 14, pp. 23-34.

59. Muday, G.K. & DeLong, A. (2001). Polar auxin transport: controlling where and how much. Trends Plant Sci., 6, pp. 535-542.

60. Peer, W.A., Blakeslee, J.J., Yang, H. & Murphy, A.S. (2011). Seven things we think we know about auxin transport. Mol. Plant, 4, No. 3, pp. 487-504.

61. Fang, Y. & Hirsch, A.M. (1998). Studying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in transgenic alfalfa. Plant Physiol., 116, No. 1, pp. 53-68.

62. Peer, W.A. & Murphy, A.S. (2007). Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci., 12, pp. 556-563.

63. Wasson, A.P., Pellerone, F.I. & Mathesius, U. (2006). Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. Plant Cell, 18, pp. 1617-1629.

64. Mathesius, U. (2001). Flavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase. J. Exp. Bot., 52, pp. 419-426.

65. Peer, W.A., Cheng, Y. & Murphy, A.S. (2013). Evidence of oxidative attenuation of auxin signaling. J. Exp. Bot., 64, pp. 2629-2639.

66. Suzaki, T., Yano, K., Ito, M., Suganuma, N. & Kawaguchi, M. (2012). Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development, 139, pp. 3997-4006.

67. Kots, S.Ya. & Gryshchuk, O.O. (2015). Phytohormones in the formation and functioning of symbiotic relationships of leguminous plants and nodule bacteria. Fiziol. rast. genet., 47, No. 3, pp. 187-206 [in Ukrainian].

68. Bladergroen, M.R. & Spaink, H.P. (1998). Genes and signal molecules involved in the rhizobia-Leguminoseae symbiosis. Plant Biology, 1, No. 4, pp. 353-359.

69. Breakspear, A., Liu, C., Roy, S., Stacey, N., Rogers, C., Trick, M., Morieri, G., Mysore, K.S., Wen, J., Oldroyd, G.E., Downie, J.A. & Murray, J.D. (2014). The root hair "infectome" of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell, 26, pp. 4680-4701.

70. Shen, C., Yue, R., Sun, T., Zhang, L., Xu, L., Tie, S., Wang, H. & Yang, Y. (2015). Genome-wide identification and expression analysis of auxin response factor gene family in Medicago truncatula. Front. Plant Sci., 6.

71. Cai, Z., Wang, Y., Zhu, L., Tian, Y., Chen, L., Sun, Z., Ullah, I. & Li, X. (2017). GmTIR1/GmAFB3-based auxin perception regulated by miR393 modulates soybean nodulation. New Phytol., 215, pp. 672-686.

72. Spaepen, S., Vanderleyden, J. & Remans, R. (2007). Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev., 31, pp. 425-448.

73. Prinsen, E., Chauvaux, N., Schmidt, J., John, M., Wieneke, U., De Greef, J., Schell, J. & Van Onckelen, H. (1991). Stimulation of indole-3-acetic acid production in Rhizobium by flavonoids. FEBS Lett., 282, pp. 53-55.

74. Theunis, M., Kobayashi, H., Broughton, W.J. & Prinsen, E. (2004). Flavonoids, NodD1, NodD2, and nod-box NB15 modulate expression of the y4wEFG locus that is required for indole-3-acetic acid synthesis in Rhizobium sp. strain NGR234. Mol. Plant-Microbe Interact., 17, pp. 1153-1161.

75. Lievens, S., Goormachtig, S., Herder, J.D., Capoen, W., Mathis, R., Hedden, P. & Holsters, M. (2005). Gibberellins are involved in nodulation of Sesbania rostrata. Plant Physiol., 139, pp. 1366-1379.

76. Ferguson, B.J., Foo, E., Ross, J.J. & Reid, J.B. (2011). Relationship between gibberellin, ethylene and nodulation in Pisum sativum. New Phytol., 189, No. 3, pp. 829-842.

77. Ferguson, B.J., Ross, J.J. & Reid, J.B. (2005). Nodulation phenotypes of gibberellin and brassinosteroid mutants of Pisum sativum. Plant Physiol., 138, pp. 2396-2405.

78. Hayashi, S., Reid, D.E., Lorenc, M.T., Stiller, J., Edwards, D., Gresshoff, P.M. & Ferguson, B.J. (2012). Transient nod factor-dependent gene expression in the nodulation-competent zone of soybean (Glycine max [L.] Merr.) roots. Plant Biotechnol. J., 10, pp. 995-1010.

79. Yoneyama, K., Xie, X., Sekimoto, H., Takeuchi, Y., Ogasawara, S., Akiyama, K., Hayashi, H. & Yoneyama, K. (2008). Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol., 179, pp. 484-494.

80. Gomez-Roldan, V., Fermas, S., Brewer, P.B., Puech-Pages, V., Dun, E.A., Pillot, J.P., Letisse, F., Matusova, R., Danoun, S., Portais, J.C., Bouwmeester, H., Becard, G., Beveridge, C., Rameau, C. & Rochange, S. (2008). Strigolactone inhibition of shoot branching. Nature, 455, pp. 189-194.

81. Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J. & Yamaguchi, S. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature, 455, pp. 195-200.

82. Foo, E. & Davies, N.W. (2011). Strigolactones promote nodulation in pea. Planta, 234, pp. 1073-1081.

83. Soto, M.J., Fernandez-Aparicio, M., Castellanos-Morales, V., Garcia-Garrido, J.M., Ocampo, J.A., Delgado, M.J. & Vierheilig, H. (2010). First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol. Biochem., 42, pp. 383-385.

84. De Cuyper, C., Fromentin, J., Yocgo, R.E., De Keyser, A., Guillotin, B., Kunert, K., Boyer, F.D. & Goormachtig, S. (2015). From lateral root density to nodule number, the strigolactone analogue GR24 shapes the root architecture of Medicago truncatula. J. Exp. Bot., 66, pp. 137-146.

85. Liu, W., Kohlen, W., Lillo, A., Op den Camp, R., Ivanov, S., Hartog, M., Limpens, E., Jamil, M., Smaczniak, C., Kaufmann, K., Yang, W.C., Hooiveld, G.J., Charnikhova, T., Bouwmeester, H.J., Bisseling, T. & Geurts, R. (2011). Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-type transcription factors NSP1 and NSP2. Plant Cell, 23, pp. 3853-3865.

86. McAdam, E.L., Hugill, C., Fort, S., Samain, E., Cottaz, S., Davies, N.W., Reid, J.B. & Foo, E. (2017). Determining the site of action of strigolactones during nodulation. Plant Physiol., 175, pp. 529-542.

87. Xie, X.N., Yoneyama, K. & Yoneyama, K. (2010). The strigolactone story. Ann. Rev. Phytopathol., 48, pp. 93-117.

88. Vasse, J., de Billy, F. & Truchet, G. (1993). Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. Plant J., 4, No. 3, pp. 555-566.

89. Stacey, G., McAlvin, C.B., Kim, S.-Y., Olivares, J. & Soto, M.J. (2006). Effects of endogenous salicylic acid on nodulation in the model legumes Lotus japonicas and Medicago truncatula. Plant Physiol., 141, pp. 1473-1481.

90. Oldroyd, G.E., Engstrom, E.M. & Long, S.R. (2001). Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell, 13, No. 8, pp. 1835-1849.

91. Sun, J., Cardoza, V., Mitchell, D.M., Bright, L., Oldroyd, G. & Harris, J.M. (2006). Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J., 46, No. 6, pp. 961-70.

92. Suzuki, A., Akune, M., Kogiso, M., Imagama, Y., Osuki, K., Uchiumi, T., Higashi, S., Han, S.Y., Yoshida, S., Asami, T. & Abe, M. (2004). Control of nodule number by the phytohormone abscisic acid in the roots of two leguminous species. Plant Cell Physiol., 45, pp. 914-922.

93. Penmetsa, R.V., Frugoli, J.A., Smith, L.S., Long, S.R. & Cook, D.R. (2003). Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol., 131, No. 3, pp. 998-1008.

94. Penmetsa, R.V., Uribe, P., Anderson, J., Lichtenzveig, J., Gish, J.C., Nam, Y.W., Engstrom, E., Xu, K., Sckisel, G., Pereira, M., Baek, J.M., Lopez-Meyer, M., Long, S.R., Harrison, M.J., Singh, K.B., Kiss, G.B. & Cook, D.R. (2008). The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. Plant J., 55, pp. 580-595.

95. Fearn, J.C. & LaRue, T.A. (1991). Ethylene inhibitors restore nodulation to sym 5 mutants of Pisum sativum L. cv. Sparkle. Plant Physiol., 96, pp. 239-244.

96. Guinel, F.C. & Sloetjes, L.L. (2000). Ethylene is involved in the nodulation phenotype of Pisum sativum R50 (sym 16), a pleiotropic mutant that nodulates poorly and has pale green leaves. J. Exp. Bot., 51, pp. 885-894.

97. Lee, K.H. & LaRue, T.A. (1992). Pleiotropic effects of sym-17: a mutation in Pisum sativum L. cv. Sparkle causes decreased nodulation, altered root and shoot growth, and increased ethylene production. Plant Physiol., 100, pp. 1326-1333.

98. Nukui, N., Ezura, H., Yuhashi, K.I., Yasuta, T. & Minamisawa, K. (2000). Effects of ethylene precursor and inhibitors for ethylene biosynthesis and perception on nodulation in Lotus japonicus and Macroptilium atropurpureum. Plant Cell Physiol., 41, pp. 893-897.

99. Caba, J.M., Recalde, L. & Ligero, F. (1998). Nitrate-induced ethylene biosynthesis and the control of nodulation in alfalfa. Plant Cell Environ, 21, pp. 87-93.

100. Guinel, F.C. & LaRue, T.A. (1992). Ethylene inhibitors partly restore nodulation to pea mutant E107 (brz). Plant Physiol., 99, pp. 515-518.

101. Markwei, C.M. & LaRue, T.A. (1997). Phenotypic characterization of sym 21, a gene conditioning shoot-controlled inhibition of nodulation in Pisum sativum cv. Sparkle. Physiol. Plant, 100, pp. 927-932.

102. Ma, W., Penrose, D.M. & Glick, B.R. (2002). Strategies used by rhizobia to lower plant ethylene levels and increase nodulation. Can. J. Microbiol., 48, No. 11, pp. 947-954.

103. Yuhashi, K.-I., Ichikawa, N., Ezura, H., Akao, S., Minakawa, Y., Nukui, N., Yasuta, T. & Minamisawa, K. (2000). Rhizobitoxine production by Bradyrhizobium elkanii enhances nodulation and competitiveness on Macroptilium atropurpureum. Appl. Environ. Microbiol., 66, pp. 2658-2663.

104. Roddam, L.F., Lewis-Henderson, W.R. & Djordjevic, M.A. (2002). Two novel chromosomal loci influence cultivar-specific nodulation failure in the interaction between strain ANU794 and subterranean clover cv. Woogenellup. Funct. Plant Biol., 29, pp. 473-483.

105. Tominaga, A., Nagata, M., Futsuki, K., Abe, H., Uchiumi, T., Abe, M., Kuc, K., Hashiguchi, M., Akashi, R., Hirsch, A., Arima, S. & Suzuki, A. (2010). Effect of abscisic acid on symbiotic nitrogen fixation activity in the root nodules of Lotus japonicus. Plant Signal. Behav., 5, No. 4, pp. 440-443.

106. Bano, A., Harper, J.E., Auge, R.M. & Neuman, D.S. (2002). Changes in phytohormone levels following inoculation of two soybean lines differing in nodulation. Funct. Plant Biol., 29, pp. 965-974.

107. Cho, M.J. & Harper, J.E. (1993). Effect of abscisic acid application on root isoflavonoid concentration and nodulation of wild-type and nodulation mutant soybean plants. Plant Soil, 153, pp. 145-149.

108. Ding, Y., Kalo, P., Yendrek, C., Sun, J., Liang, Y., Marsh, J.F., Harris, J.M. & Oldroyd, G.E. (2008). Abscisic acid coordinates Nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant Cell, 20, pp. 2681-2695.

109. Wu, Y., Sanchez, J.P., Lopez-Molina, L., Himmelbach, A., Grill, E. & Chua, N.H. (2003). The abi1-1 mutation blocks ABA signaling downstream of cADPR action. Plant J., 34, pp. 307-315.

110. Caba, J.M., Centeno, M.L., Fernandez, B., Gresshoff, P.M. & Ligero, F. (2000). Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type. Planta, 211, pp. 98-104.

111. Gonzalez, E.M., Galvez, L. & Arrese-Igor, C. (2001). Abscisic acid induces a decline in nitrogen fixation that involves leghaemoglobin, but is independent of sucrose synthase activity. J. Exp. Bot., 52, pp. 285-293.

112. Tominaga, A., Nagata, M., Futsuki, K., Abe, H., Uchiumi, T., Abe, M., Kucho, K., Hashiguchi, M., Akashi, R., Hirsch, A.M., Arima, S. & Suzuki, A. (2009). Enhanced nodulation and nitrogen fixation in the abscisic acid low-sensitive mutant enhanced nitrogen fixation1 of Lotus japonicus. Plant Physiol., 151, No. 4, pp. 1965-1976.

113. Gonzalez, E.M., Galvez, L., Royuela, M., Aparicio-Tejo, P.M. & Arrese-Igor, C. (2001). Insights into the regulation of nitrogen fixation in pea nodules: lessons from drought, abscisic acid and increased photoassimilate availability. Agronomie, 21, pp. 607-613.

114. Trinchant, J.C. & Rigaud, J. (1982). Nitrite and nitric oxide as inhibitors of nitrogenase from soybean bacteroids. Appl. Environ. Microbiol., 44, pp. 1385-1388.

115. Garcia-Mata, C. & Lamattina, L. (2002). Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol., 128, pp. 790-792.

116. Gryshchuk, O.O. (2014). Phytohormonal status of soybean plants at use of strains with different symbiotic characteristics. Avtoref. dys. … kand. biol nauk. Kyiv, 21 p. [in Ukrainian].

117. Gryshchuk, O.O., Volkogon, M.V. & Kots, S.Ya. (2012). The dynamics of indolil-3-acetic and abscisic acids content in roots and nodules of soybean on the early stages of legume-rhizobiun symbiosis. Fiziologiya i biohimiya kult. rasteniy, 41, No. 5, pp. 408-416 [in Ukrainian].

118. Nakagawa, T. & Kawaguchi, M. (2006). Shoot-applied MeJA suppresses root nodulation in Lotus japonicas. Plant Cell Physiol., 47, pp. 176-180.

119. Kinkema, M. & Gresshoff, P.M. (2008). Investigation of downstream signals of the soybean autoregulation of nodulation receptor kinase GmNARK. Mol. Plant-Microbe Interact., 21, pp. 1337-1348.

120. Seo, H.S., Li, J., Lee, S.-Y., Yu, J.W., Kim, K.H., Lee, S.H., Lee, I.J. & Paek, N.C. (2007). The hypernodulating nts mutation induces jasmonate synthetic pathway in soybean leaves. Mol. Cells, 24, pp. 185-193.

121. Mabood, F. & Smith, D.L. (2005). Pre-inoculation of Bradyrhizobium japonicum with jasmonates accelerates nodulation and nitrogen fixation in soybean (Glycine max) at optimal and suboptimal root zone temperatures. Physiol. Plant, 125, pp. 311-323.

122. Rosas, S., Soria, R., Correa, N. & Abdala, G. (1998). Jasmonic acid stimulates the expression of nod genes in Rhizobium. Plant Mol. Biol., 38, pp. 1161-1168.

123. Mabood, F., Souleimanov, A., Khan, W. & Smith, D.L. (2006). Jasmonates induce Nod factor production by Bradyrhizobium japonicum. Plant Physiol. Biochem., 44, pp. 759-765.

124. Poustini, K., Mabood, F. & Smith, D.L. (2005). Low root zone temperature effects on bean (Phaseolus vulgaris L.) plants inoculated with Rhizobium leguminosarum bv. phaseoli pre-incubated with methyl jasmonate and/or genistein. ACTA AGR SCAND B-S P., 55, pp. 293-298.

125. Martinez-Abarca, F., Herrera-Cervera, J.A., Bueno, P., Sanjuan, J., Bisseling, T. & Olivares, J. (1998). Involvement of salicylic acid in the establishment of the Rhizobium meliloti-alfalfa symbiosis. Mol. Plant-Microbe Interact., 11, pp. 153-155.

126. Maekawa, T., Maekawa-Yoshikawa, M., Takeda, N., Imaizumi-Anraku, H., Murooka, Y. & Hayashi, M. (2009). Gibberellin controls the nodulation signaling pathway in Lotus japonicas. Plant J., 58, pp. 183-194.

127. Nutman, P.S. (1952). Studies on the physiology of nodule formation. III. Experiments on the excision of root-tips and nodules. Ann. Bot., 16, pp. 79-103.

128. Nontachaiyapoom, S., Scott, P.T., Men, A.E., Kinkema, M., Schenk, P.M. & Gresshoff, P.M. (2007). Promoters of orthologous Glycine max and Lotus japonicus nodulation autoregulation genes interchangeably drive phloem-specific expression in transgenic plants. Mol. Plant-Microbe Interact., 20, pp. 769-780

129. Suzaki, T., Yoro, E. & Kawaguchi, M. (2015). Leguminous plants: inventors of root nodules to accommodate symbiotic bacteria. Int. Rev. Cell Mol. Biol., 316, pp. 111-158.

130. Okamoto, S., Tabata, R. & Matsubayashi, Y. (2016). Long-distance peptide signaling essential for nutrient homeostasis in plants. Curr. Opin. Plant Biol., 34, pp. 35-40.

131. Nishida, H. & Suzaki, T. (2018). Two negative regulatory systems of root nodule symbiosis — how are symbiotic benefits and costs balanced? Plant Cell Physiol., 59, No. 9, pp. 1733-1738.

132. Okamoto, S., Ohnishi, E., Sato, S., Takahashi, H., Nakazono, M., Tabata, S. & Kawaguchi, M. (2009). Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol., 50, pp. 67-77.

133. Nishida, H., Handa, Y., Tanaka, S., Suzaki, T. & Kawaguchi, M. (2016). Expression of the CLE-RS3 gene suppresses root nodulation in Lotus japonicus. J. Plant Res., 129, pp. 909-919.

134. Mortier, V., Den Herder, G., Whitford, R., Van de Velde, W., Rombauts, S., D'Haeseleer, K., Holsters, M. & Goormachtig, S. (2010). CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol., 153, pp. 222-237.

135. Nishida, H., Tanaka, S., Handa, Y., Ito, M., Sakamoto, Y., Matsunaga, S., Betsuyaku, S., Miura, K., Soyano, T., Kawaguchi, M. & Suzaki, T. (2018). A NIN-LIKE PROTEIN mediates nitrate-induced control of root nodule symbiosis in Lotus japonicus. Nat. Commun., 9, No. 499.

136. Soyano, T., Hirakawa, H., Sato, S., Hayashi, M. & Kawaguchi, M. (2014). Nodule inception creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production. Proc. Natl. Acad. Sci. USA, 111, pp. 14607-14612.

137. Miyazawa, H., Oka-Kira, E., Sato, N., Takahashi, H., Wu, G.-J., Sato, S., Hayashi, M., Betsuyaku, S., Nakazono, M., Tabata, S., Harada, K., Sawa, S., Fukuda, H. & Kawaguchi, M. (2010). The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus. Development, 137, pp. 4317-4325.

138. Okamoto, S., Shinohara, H., Mori, T., Matsubayashi, Y. & Kawaguchi, M. (2013). Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat. Commun., 4, No. 2191.

139. Sasaki, T., Suzaki, T., Soyano, T., Kojima, M., Sakakibara, H. & Kawaguchi, M. (2014). Shoot-derived cytokinins systemically regulate root nodulation. Nat. Commun., 5, No. 4983.

140. Azarakhsh, M., Lebedeva, M.A. & Lutova, L.A. (2018). Identification and expression analysis of Medicago truncatula isopentenyl transferase genes (IPTs) involved in local and systemic control of nodulation. Front. Plant Sci., 9, No. 304.

141. Takahara, M., Magori, S., Soyano, T., Okamoto, S., Yoshida, C., Yano, K., Sato, S., Tabata, S., Yamaguchi, K., Shigenobu, S., Takeda, N., Suzaki, T. & Kawaguchi, M. (2013). TOO MUCH LOVE, a novel Kelch repeat-containing F-box protein, functions in the long-distance regulation of the legume-rhizobium symbiosis. Plant Cell Physiol., 54, pp. 433-447.

142. Den Herder, G. & Parniske, M. (2009). The unbearable naivety of legumes in symbiosis. Curr. Opin. Plant Biol., 12, pp. Foo, E. & Davies, N.W. (2011). Strigolactones promote nodulation in pea. Planta, 234, pp. 1073-1081.