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Regulation of Legume-Rhizobial Symbiosis: Molecular Genetic Aspects and Participation of Reactive Oxygen Species

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Abstract

The formation of legume-rhizobial symbiosis goes through a series of coordinated stages, the main of which is the distant interaction of symbionts, which is carried out through the exchange of molecular signals between macro- and microsymbionts. There is clear regulation in the interaction between symbiosis partners: rhizobia with their associated molecular patterns (MAMPs) and the plant, which forms two types of immune response (MTI/ETI) to infection, leading to the activation of symbiotic processes in host plants and suppression of their functional systems. The development of protective reactions of legume plants to the invasion of rhizobia is very similar to the processes of pathogenesis. However, the result of symbiotic interaction is not the inactivation of the microorganism but rather the regulation of its reproduction and metabolic activity, primarily regulated by macrosymbionts. Clear regulation of precontact intermolecular events between both partners of symbiosis leads to the activation of the main pathways of symbiotic signals’ transduction and the successful development of organogenesis programs of the nodule–epidermal and cortical. The important participation of the reactive oxygen species in the regulation of symbiotic processes that occur on the early stages of interaction of macro- and microsymbionts (preinfection, infection, formation of infectious threads), as well as the prospects for further studies of these signaling molecules in integration with other transduction pathways of legume-rhizobial symbiosis formation, were highlighted. The review summarizes the current scientific information on the main molecular genetic mechanisms that underlie the regulation of symbiotic interaction of legumes with nodule bacteria as well as the participation of reactive oxygen species in the formation of legume-rhizobial symbiosis.

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REFERENCES

  1. Andrio, E., Marino, D., Marmeys, A., et al., Hydrogen peroxide-regulated genes in the Medicago truncatulaSinorhizobium meliloti symbiosis, New Phytol., 2013, vol. 198, no. 1, pp. 179–189. https://doi.org/10.1111/nph.12120

    Article  PubMed  Google Scholar 

  2. Bagam, P., Singh, D.P., Inda, M.E., and Batra, S., Unraveling the role of membrane microdomains during microbial infection, Cell Biol. Toxicol., 2017, vol. 33, no. 5, pp. 429–455. https://doi.org/10.1007/s10565-017-9386-9

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bao, Y. and Howell, S.H., The unfolded protein response supports plant development and defense as well as responses to abiotic stress, Front. Plant Sci., 2017, vol. 8, p. 344. https://doi.org/10.3389/fpls.2017.00344

    Article  PubMed  PubMed Central  Google Scholar 

  4. Berrabah, F., Ratet, P., and Gourion, B., Multiple steps control immunity during the intracellular accommodation of rhizobia, J. Exp. Bot., 2015, vol. 66, pp. 1977–1985. https://doi.org/10.1093/jxb/eru545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Binder, A. and Parniske, M., Analysis of the Lotus japonicus nuclear pore NUP107-160 subcomplex reveals pronounced structural plasticity and functional redundancy, Front. Plant Sci., 2014, vol. 4, p. 552. https://doi.org/10.3389/fpls.2013.00552

    Article  PubMed  PubMed Central  Google Scholar 

  6. Braun, D.A., Khokha, M.K., and Hildebrandt, F., Mutations in multiple components of the nuclear pore complex cause nephrotic syndrome, J. Clin. Invest., 2018, vol. 128, no. 10, pp. 4313–4328. https://doi.org/10.1172/JCI98688

    Article  PubMed  PubMed Central  Google Scholar 

  7. Cao, Y., Halane, M.K., Gassmann, W., and Stacey, G., The role of plant innate immunity in the legume–Rhizobium symbiosis, Annu. Rev. Plant Biol., 2017, vol. 68, pp. 535–561. https://doi.org/10.1146/annurev-arplant-042916-041030

    Article  CAS  PubMed  Google Scholar 

  8. Cardenas, L., Martinez, A., Sanchez, F., and Quinto, C., Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs), Plant J., 2008, vol. 56, no. 5, pp. 802–813. https://doi.org/10.1111/j.1365-313X.2008.03644.x

    Article  CAS  PubMed  Google Scholar 

  9. Cerri, M.R.., Frances, L., Laloum, T., et al., Medicago truncatula ERN transcription factors: regulatory interplay with NSP1/NSP2 GRAS factors and expression dynamics throughout rhizobial infection, Plant Physiol., 2012, vol. 160, pp. 2155–2172. https://doi.org/10.1104/pp.112. 203190

  10. Chen, C., Fan, C., Gao, M., and Zhu, H., Antiquity and function of CASTOR and POLLUX, the twin ion channel-encoding genes key to the evolution of root symbioses in plants, Plant Physiol., 2009, vol. 149, no. 1, pp. 306–317. https://doi.org/10.1104/pp.108.131540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Chou, K.C. and Shen, H.B., Plant-mPLoc: a top–down strategy to augment the power for predicting plant protein subcellular localization, PLoS One, 2010, vol. 5, no. 6, e11335. https://doi.org/10.1371/journal.pone.0011335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Cho, Y.H. and Yoo, S.D., Novel connections and gaps in ethylene signaling from the ER membrane to the nucleus, Front. Plant Sci., 2015, vol. 5, p. 733. https://doi.org/10.3389/fpls.2014.00

    Article  PubMed  PubMed Central  Google Scholar 

  13. Combier, J.P., Frugier, F., and de Billy, F., MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula, Genes Dev., 2006, vol. 20, no. 22, pp. 3084–3088. https://doi.org/10.1101/gad.402806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Costa, A., Drago, I., Behera, S., et al., H2O2 in plant peroxisomes: an in vivo analysis uncovers a Ca2+-dependent scavenging system, Plant J., 2010, vol. 62, no. 5, pp. 760–772. https://doi.org/10.1111/j.1365-313X.2010.04190.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Czarnocka, W. and Karpinski, S., Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses, Free Radical Biol. Med., 2018, vol. 122, pp. 4–20. https://doi.org/10.1016/j.freeradbiomed.2018.01.011

    Article  CAS  Google Scholar 

  16. Damiani, I., Drain, A., and Guichard, M., Nod factor effects on root hair-specific transcriptome of Medicago truncatula: focus on plasma membrane transport systems and reactive oxygen species networks, Front. Plant Sci., 2016, vol. 7, p. 794. https://doi.org/10.3389/fpls.2016.00794

    Article  PubMed  PubMed Central  Google Scholar 

  17. Desbrosses, G.J. and Stougaard, J., Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways, Cell Host Microbe, 2011, vol. 10, no. 4, pp. 348–358. https://doi.org/10.1016/j.chom.2011.09.005

    Article  CAS  PubMed  Google Scholar 

  18. Fonouni-Farde, C., Kisiala, A., Brault, M., et al., DELLA1-mediated gibberellin signaling regulates cytokinin-dependent symbiotic nodulation, Plant Physiol., 2017, vol. 175, no. 4, pp. 1795–1806. https://doi.org/10.1104/pp.17.00919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Gamas, P., Brault, M., Jardinaud, M.F., and Frugier, F., Cytokinins in symbiotic nodulation: when, where, what for?, Trends Plant Sci., 2017, vol. 22, no. 9, pp. 792–802. https://doi.org/10.1016/j.tplants.2017.06.012

    Article  CAS  PubMed  Google Scholar 

  20. Garbetta, D. and Bretscher, A., The surprising dynamics of scaffolding proteins, Mol. Biol. Cell, 2014, vol. 25, no. 16, pp. 2315– 2319. https://doi.org/10.1091/mbc.E14-04-0878

    Article  CAS  Google Scholar 

  21. Glyanko, A.K., Defensive mechanisms of rhizobia-infected legume plants, Visn. Hark. Nac. Agrar. Univ., Ser. Biol., 2016, vol. 1, no. 37, pp. 63–77.

    Google Scholar 

  22. Gourion, B., Berrabah, F., Ratet, P., and Stacey, G., Rhizobium–legume symbioses: the crucial role of plant immunity, Trends Plant Sci., 2015, vol. 20, no. 3, pp. 186–194. https://doi.org/10.1016/j.tplants.2014.11.008

    Article  CAS  PubMed  Google Scholar 

  23. Groth, M., Takeda, N., Perry, J., et al., NENA, a Lotus japonicas homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development, Plant Cell, 2010, vol. 22, pp. 2509– 2526. https://doi.org/10.1105/tpc.109.069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Groten, K., Vanacker, H., Duttileul, C., et al., The roles of redox processes in pea nodule development and senescence, Plant, Cell Environ., 2005, vol. 28, pp. 1293–1304. https://doi.org/10.1111/j.1365-3040.2005.01376.x

    Article  CAS  Google Scholar 

  25. Guinel, F., Getting around the legume nodule: I. The structure of the peripheral zone in four nodule types, Botany, 2009a, vol. 87, pp. 1117–1138. https://doi.org/10.1139/b09-074

    Article  Google Scholar 

  26. Guinel, F.C., Getting around the legume nodule: II. Molecular biology of its peripheral zone and approaches to study its vasculature, Botany, 2009b, vol. 87, pp. 1139–1166. https://doi.org/10.1139/b09-075

    Article  Google Scholar 

  27. Haney, C.H. and Long, S.R., Plant flotillins are required for infection by nitrogen-fixing bacteria, Proc. Natl. Acad. Sci. U. S. A., 2010, vol. 107, no. 1, pp. 478–483. https://doi.org/10.1073/pnas.0910081107

    Article  PubMed  Google Scholar 

  28. Harrison, J., Jamet, A., Muglia, C.I., et al., Glutathione plays a fundamental role in growth and symbiotic capacity of Sinorhizobium meliloti, J. Bacteriol., 2005, vol. 187, no. 1, pp. 168–174. https://doi.org/10.1128/JB.187.1.168-174.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Hasanuzzaman, M., Bhuyan, M.H., Zulfiqar, F., et al., Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator, Antioxidants (Basel), 2020, vol. 9, no. 8, p. 681. https://doi.org/10.3390/antiox9080681

    Article  CAS  PubMed Central  Google Scholar 

  30. Hastwell, A.H., Gresshoff, P.M., and Ferguson, B.J., The structure and activity of nodulation-suppressing CLE peptide hormones of legumes, Funct. Plant Biol., 2014, vol. 42, no. 3, pp. 229–238. https://doi.org/10.1071/FP14222

    Article  CAS  Google Scholar 

  31. Hayashi, T., Banba, M., Shimoda, Y., et al., A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts, Plant J., 2010, vol. 63, pp. 141–154. https://doi.org/10.1111/j.1365-313X.2010. 04228.x

  32. Hirsch, S. and Oldroyd, G.E.D., GRAS-domain transcription factors that regulate plant development, Plant Signal. Behav., 2014, vol. 4, no. 8, pp. 698–700. https://doi.org/10.4161/psb.4.8.9176

    Article  Google Scholar 

  33. Hoffmann-Sommergruber, K., Pathogenesis-related (PR)-proteins identified as allergens, Biochem. Soc. Trans., 2002, vol. 30, no. 6, pp. 930–935. https://doi.org/10.1042/bst0300930

    Article  CAS  PubMed  Google Scholar 

  34. Hossain, Md.S., Liao, J., James, E.K., et al., Lotus japonicus ARPC1 is required for rhizobial infection, Plant Physiol., 2012, vol. 160, no. 2, pp. 917–928. https://doi.org/10.1104/pp.112. 202572

  35. Jamet, A., Mandon, K., Puppo, A., and Herouart, D., H2O2 is required for optimal establishment of the Medicago sativa/Sinorhizobium meliloti symbiosis, J. Bacteriol., 2007, vol. 189, no. 23, pp. 8741–8745. https://doi.org/10.1128/JB.01130-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Jin, Y., Liu, H., Luo, D., et al., DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways, Nat. Commun., 2016, vol. 7, p. 12433. https://doi.org/10.1038/ncomms12433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Jin, J.H., Wang, M., Zhang, H.X., et al., Genome-wide identification of the AP2/ERF transcription factor family in pepper (Capsicum annuum L.), Genome, 2018, vol. 61, no. 9, pp. 663–674. https://doi.org/10.1139/gen-2018-0036

    Article  CAS  PubMed  Google Scholar 

  38. Inzieze, A., Vanderauwera, S., Hoeberichts, F.A., et al., A subcellular localization compendium of hydrogen peroxide-induced proteins, Plant, Cell Environ., 2011, vol. 35, no. 2, pp. 308–320. https://doi.org/10.1111/j.1365-3040. 2011.02323.x

  39. Kawaharada, Y., Kelly, S., Wibroe, N.M., et al., Receptor-mediated exopolysaccharide perception controls bacterial infection, Nature, 2015, vol. 523, pp. 308–312. https://doi.org/10.1038/nature14611

  40. Kawaharada, Y., James, E.K., Kelly, S., et al., The ethylene responsive factor required for nodulation 1 (ERN1) transcription factor is required for infection-thread formation in Lotus japonicas, Mol. Plant Microbe Interact., 2017, no. 3, pp. 194–204. https://doi.org/10.1094/MPMI-11-16-0237-R

  41. Khafi, A.S., Iranbakhsh, A., Afshar, A.S., et al., RBOH expression and ROS metabolism in Citrullus colocynthis under cadmium stress, Braz. J. Bot., 2020, vol. 43, no. 1, vol. 35–43. https://doi.org/10.1007/s40415-020-00581-z

  42. Kim, S., Zeng, W., Svet, B., et al., Ca2+-regulated Ca2+ channels with an RCK gating ring control plant symbiotic associations, Nat. Commun., 2019, vol. 10, no. 3703, pp. 1–12. https://doi.org/10.1038/s41467-019-11698-5

    Article  CAS  Google Scholar 

  43. Kim, E.J., Kim, Y.J., Hong, W.J., et al., Genome-wide analysis of root hair preferred RBOH genes suggests that three RBOH genes are associated with auxin-mediated root hair development in rice, J. Plant Biol., 2019, vol. 62, no. 3, pp. 229–238. https://doi.org/10.1007/s12374-019-0006-5

    Article  CAS  Google Scholar 

  44. Kirienko, A.N., Porozov, Y.B., Malkov, N.V., et al., Role of a receptor-like kinase K1 in pea–Rhizobium symbiosis development, Planta, 2018, vol. 248, no. 5, pp. 1101–1120.https://doi.org/10.1007/s00425-018-2944-4

    Article  CAS  PubMed  Google Scholar 

  45. Kosuta, S., Held, M., Hossain, M.S., et al., Lotus japonicus symRK-14 uncouples the cortical and epidermal symbiotic program, Plant J., 2011, vol. 67, no. 5, pp. 929–940. https://doi.org/10.1111/j.1365-313X.2011.04645.x

    Article  CAS  PubMed  Google Scholar 

  46. Kots, S.Ya. and Hryshchuk, O.O., Phytohormonal regulation of legume–Rhizobium symbiosis, Fiziol. Rast. Genet., 2019, vol. 51, no. 1, pp. 1–27. https://doi.org/10.15407/frg 2019.01.003

  47. Kots, S.Ya., Mamenko, T.P., and Khomenko, Yu.A., The content of hydrogen peroxide and catalase activity in different on effectiveness of symbiotic systems Glycine maxBradyrhizobium japonicum under drought conditions, Mikrobiol. Z., 2019, vol. 81, no. 4, pp. 65–72. https://doi.org/10.15407/microbiolj81.04.062

    Article  Google Scholar 

  48. Kumar, S., Kumar, A., Mamidi, P., et al., Chikungunya virus nsP1 interacts directly with nsP2 and modulates its ATPase activity, Sci. Rep., 2018, vol. 8, no. 1, p. 1045. https://doi.org/10.1038/s41598-018-19295-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Laffont, C., Ivanovici, A., Gautrat, P., et al., The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically, Nat. Commun., 2020, vol. 11, p. 3167. https://doi.org/10.1038/s41467-020-16968-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lang, C. and Long, S.R., Transcriptomic analysis of Sinorhizobium meliloti and Medicago truncatula symbiosis using nitrogen fixation-deficient nodules, Mol. Plant Microbe Intract., 2015, vol. 28, no. 8, pp. 856–868. https://doi.org/10.1094/MPMI-12-14-0407-R

    Article  CAS  Google Scholar 

  51. Laxa, M., Liebthal, M., Telman, W., et al., The role of the plant antioxidant system in drought tolerance, Antioxidants (Basel), 2019, vol. 8, no. 4, pp. 1–31. https://doi.org/10.3390/an-tiox8040094

    Article  Google Scholar 

  52. Lefebvre, B., Timmers, T., Mbengue, M., et al., A remorin protein interacts with symbiotic receptors and regulates bacterial infection, Proc. Natl. Acad. Sci. U. S. A., 2010, vol. 107, no. 5, pp. 2343– 2348. https://doi.org/10.1073/pnas.0913320107

    Article  PubMed  PubMed Central  Google Scholar 

  53. Li, H., Chen, M., Duan, L., et al., Domain swap approach reveals the critical roles of different domains of SYMRK in root nodule symbiosis in Lotus japonicus, Front. Plant Sci., 2018, vol. 9, pp. 1–10. https://doi.org/10.3389/fpls.2018.00697

    Article  Google Scholar 

  54. Limpens, E., van Zeijl, A., and Geurts, R., Lipochitooligosaccharides modulate plant host immunity to enable endosymbiosis, Annu. Rev. Phytopathol., 2015, vol. 53, pp. 151–154. https://doi.org/10.1146/annurev-phyto-080614-120149

    Article  CAS  Google Scholar 

  55. Liu, J. and Bisseling, T., Evolution of NIN and NIN-like genes in relation to nodule symbiosis, Genes, 2020, vol. 11, pp. 1–15. https://doi.org/10.3390/genes11070777

    Article  CAS  Google Scholar 

  56. Liu, M., Soyano, T., Yano, K., et al., ERN1 and CYCLOPS coordinately activate NIN signaling to promote infection thread formation in Lotus japonicas, J. Plant Res., 2019, vol. 132, no. 5, pp. 641–653. https://doi.org/10.1007/s10265-019-01122-w

    Article  CAS  PubMed  Google Scholar 

  57. Liu, H., Zhang, C., Yang, J., et al., Hormone modulation of legume–rhizobial symbiosis, Integr. Plant Biol., 2018, vol. 60, no. 8, pp. 632–648. https://doi.org/10.1111/jipb.12653

    Article  CAS  Google Scholar 

  58. Lohar, D.P., Haridas, S., and Gantt, J.S., A transient decrease in reactive oxygen species in roots leads to root hair deformation in the legume–rhizobia symbiosis, New Phytol., 2007, vol. 173, no. 1, pp. 39–49. https://doi.org/10.1111/j.1469-8137.2006.01901.x

    Article  CAS  PubMed  Google Scholar 

  59. Lopez-Gomez, M., Sandal, N., Stougaard, J., and Boller, T., Interplay of flg22-induced defence responses and nodulation in Lotus japonicus, J. Exp. Bot., 2012, vol. 63, pp. 393–401. https://doi.org/10.1093/jxb/err291

    Article  CAS  PubMed  Google Scholar 

  60. Mamenko, T.P., Khomenko, Yu.O., and Kots, S.Ya., Activity of superoxide dismutase and enzymes of ascorbate-glutathione cycle in Glycine maxBradyrhizobium japonicum symbiotic systems with action drought, Mikrobiol. Z., 2018, vol. 80, no. 3, pp. 77–88. https://doi.org/10.15407/microbiolj80.03.077

    Article  Google Scholar 

  61. Mamenko, T.P., Khomenko, Y.O., and Kots, S.Y., Influence of fungicides on activities of enzymes of phenolic metabolism in the early stages of formation and functioning of soybean symbiotic apparatus, Regul. Mech. Biosyst., 2019, vol. 10, no. 1, pp. 111–116. https://doi.org/10.15421/021917

    Article  Google Scholar 

  62. Marino, D., Andrio, E., Danchin, E.G.J., et al., A Medicago truncatula NADPH oxidase is involved in symbiotic nodule functioning, New Phytol., 2011, vol. 189, no. 2, pp. 580–592. https://doi.org/10.1111/j.1469-8137.2010.03509.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Marino, D., Dunand, C., Puppo, A., and Pauly, N., A burst of plant NADPH oxidases, Trends Plant Sci., 2012, vol. 17, no. 1, pp. 9–15. https://doi.org/10.1016/j.tplants.2011.10.001

    Article  CAS  PubMed  Google Scholar 

  64. Matamoros, M.A., Dalton, D.A., Ramos, J., et al., Biochemistry and molecular biology of antioxidants in the rhizobia–legume symbiosis, Plant Physiol., 2003, vol. 133, no. 2, pp. 499–509. https://doi.org/10.1104/pp.103.025619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Mbengue, M., Camut, S., de Carvalho-Niebel, F., et al., The Medicago truncatula E3 ubiquitin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation, Plant Cell, 2010, vol. 22, pp. 3471–3488. https://doi.org/10.11105/tpc.110.075861

    Article  Google Scholar 

  66. Mhamdi, A. and Van Breusegem, F., Reactive oxygen species in plant development, Development, 2018, vol. 145, no. 15, pp. 1–12. https://doi.org/10.1242/dev.164376

    Article  CAS  Google Scholar 

  67. Mittler, R., Vanderauwera, S., Suzuki, N., et al., ROS signaling: the new wave?, Trends Plant Sci., 2011, vol. 16, pp. 300–309. https://doi.org/10.1016/j.tplants.2011.03.007

    Article  CAS  PubMed  Google Scholar 

  68. Miyata, K., Kawaguchi, M., and Nakagawa, T., Two distinct EIN2 genes cooperatively regulate ethylene signaling in Lotus japonicus, Plant Cell Physiol., 2013, vol. 54, pp. 1469–1477. https://doi.org/10.1093/pcp/pct095

    Article  CAS  PubMed  Google Scholar 

  69. Miyahara, A., Richens, J., Starker, C., et al., Conservation in function of a SCAR/WAVE component during infection thread and root hair growth in Medicago truncatula, Mol. Plant–Microbe Interact., 2010, vol. 23, no. 12, pp. 1553–1562. https://doi.org/10.1094/MPMI-06-10-0144

    Article  CAS  PubMed  Google Scholar 

  70. Montiel, J., Nava, N., Cardenas, L., et al., Phaseolus vulgaris NADPH oxidase gene is required for root infection by rhizobia, Plant Cell Physiol., 2012, vol. 53, no. 10, pp. 1751–1767. https://doi.org/10.1093/pcp/pcs120

    Article  CAS  PubMed  Google Scholar 

  71. Morgun, V.V., Kots, S.Ya., Mamenko, T.P., and Vorobey, N.A., Lipid peroxidation intensity in different on effectiveness of symbiotic systems Glycine maxBradyrhizobium japonicum under drought conditions, Mikrobiol. Z., 2020, vol. 82, no. 4, pp. 23–30. https://doi.org/10.15407/microbi-olj82.04.023

    Article  Google Scholar 

  72. Murray, J.D., Invasion by invitation: rhizobial infection in legumes, Mol. Plant– Microbe Interact., 2011, vol. 24, no. 6, pp. 631–639. https://doi.org/10.1094/MPMI-08-10-0181

    Article  CAS  PubMed  Google Scholar 

  73. Murray, J.D., Muni, R.R.D., Torres-Jerez, I., et al., Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula, Plant J., 2011, vol. 65, no. 2, pp. 244–252. https://doi.org/10.1111/j.1365-313X.2010.04415.x

    Article  CAS  PubMed  Google Scholar 

  74. Nakagawa, T., Kaku, H., Shimoda, Y., et al., From defense to symbiosis: limited alterations in the kinase domain of LysM receptor-like kinases are crucial for evolution of legume–Rhizobium symbiosis, Plant J., 2011, vol. 65, pp. 169–180. https://doi.org/10.1111/j.1365-313X.2010.04411.x

    Article  CAS  PubMed  Google Scholar 

  75. Nanda, A.K., Andrio, E., Marino, D., et al., Reactive oxygen species during plant–microorganism early interactions, J. Integr. Plant Biol., 2010, vol. 52, no. 2, pp. 195–204. https://doi.org/10.1111/j.1744-7909.2010.00933.x

    Article  CAS  PubMed  Google Scholar 

  76. Nishida, H., Tanaka, S., Handa, Y., et al., NIN-LIKE PROTEIN mediates nitrate-induced control of root nodule symbiosis in Lotus japonicus, Nat. Commun., 2018, vol. 9, no. 1, p. 499. https://doi.org/10.1038/s41467-018-02831-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Noctor, G., Reichheld, J.P., and Foyerd, C.H., ROS-related redox regulation and signaling in plants, Semin. Cell Dev. Biol., 2018, vol. 80, pp. 3–12. https://doi.org/10.1016/j.semcdb.2017.07.013

    Article  CAS  PubMed  Google Scholar 

  78. Oldroyd, G.E.D., Speak, friend, and enter: signalling systems that promote beneficial associations in plants, Nat. Rev., 2013, vol. 11, pp. 252–263. https://doi.org/10.1038/nrmicro2990

    Article  CAS  Google Scholar 

  79. Oldroyd, G.E., Murray, J.D., Poole, P.S., and Downie, J.A., The rules of engagement in the legume–rhizobial symbiosis, Annu. Rev. Genet., 2011, vol. 45, pp. 119–144. https://doi.org/10.1146/annurev-genet-110410-132549

    Article  CAS  PubMed  Google Scholar 

  80. Ott, T., Membrane nanodomains and microdomains in plant–microbe interactions, Curr. Opin. Plant Biol., 2017, vol. 40, pp. 82–88. https://doi.org/10.1016/j.pbi.2017.08.008

    Article  CAS  PubMed  Google Scholar 

  81. Pavlyshche, A.V., Mamenko, T.P., Rybachenko, L.I., and Kots, S.Ya., Influence of fungicides on the formation, function and peroxidase activity of root soybean nodules at inoculation by rhizobia incubated with lectin, Mikrobiol. Z., 2018, vol. 80, no. 5, pp. 76–89. https://doi.org/10.15407/microbiolj80.05.076

    Article  Google Scholar 

  82. Plet, J., Wasson, A., Ariel, F., et al., MtCRE1-depen-dent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula, Plant J., 2011, vol. 65, no. 4, pp. 622–633. https://doi.org/10.1111/j.1365-313X.2010.04447.x

    Article  CAS  PubMed  Google Scholar 

  83. Pongsilp, N. and Nimnoi, P., Inoculation of Ensifer fredii strain LP2/20 immobilized in agar results in growth promotion and alteration of bacterial community structure of Chinese kale planted soil, Sci. Rep., 2020, vol. 10, p. 15857. https://doi.org/10.1038/s41598-020-72986-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Ramu, S.K., Peng, H.M., and Cook, D.R., Nod factor induction of reactive oxygen species is correlated with expression of the early nodulin gene rip1 in Medicago truncatula, Mol. Plant–Microbe Interact., 2002, vol. 15, no. 6, pp. 522–528. https://doi.org/10.1094/MPMI.2002.15.6.522

    Article  CAS  PubMed  Google Scholar 

  85. Saha, S., Paul, A., Herring, L., et al., Gatekeeper tyrosine phosphorylation of SYMRK is essential for synchronizing the epidermal and cortical responses in root nodule symbiosis, Plant Physiol., 2016, vol. 171, pp. 71–81. https://doi.org/10.1104/pp.15.01962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Salanenka, Y., Verstraeten, I., Lofke, C., et al., Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane, Proc. Natl. Acad. Sci. U. S. A., 2018, vol. 115, no. 14, pp. 3716– 3721. https://doi.org/10.1073/pnas.1721760115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Santos, R., Herouart, D., Puppo, A., and Touati, D., Critical protective role of bacterial superoxide dismutase in Rhizobium–legume symbiosis, Mol. Microbiol., 38(4):750–759. https://doi.org/10.1046/j.1365-2958.2000. 02178.x

  88. Schaller, A., Stintzi, A., and Graff, L., Subtilases—versatile tools for protein turnover, plant development, and interactions with the environment, Physiol. Plant., 2012, vol. 145, no. 1, pp. 52–66. https://doi.org/10.1111/j.1399-3054 2011.01529.x

  89. Schwember, A.R., Schulze, J., Del, P.A., and Cabeza, R.A., Regulation of symbiotic nitrogen fixation in legume root nodules, Plants (Basel), 2019, vol. 8, no. 9, p. 333. https://doi.org/10.3390/plants8090333

    Article  CAS  PubMed Central  Google Scholar 

  90. Segal, L.M. and Wilson, R., Reactive oxygen species metabolism and plant–fungal interactions, Fungal Genet. Biol., 2018, vol. 110, pp. 1–9. https://doi.org/10.1016/j.fgb.2017.12.003

    Article  CAS  PubMed  Google Scholar 

  91. Shaw, S.L. and Long, S.R., Nod factor inhibition of reactive oxygen efflux in a host legume, Plant Physiol., 2003, vol. 132, no. 4, pp. 2196–2204. https://doi.org/10.1104/pp.103.021113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Sidhu, N.S., Pruthi, G., Singh, S., et al., Genome-wide identification and analysis of GRAS transcription factors in the bottle gourd genome, Sci. Rep., 2020, vol. 10, p. 14338. https://doi.org/10.1038/s41598-020-71240-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Sierla, M., Waszczak, C., Vahisalu, T., and Kangasjrvi, J., Reactive oxygen species in the regulation of stomatal movements, Plant Physiol., 2016, vol. 171, no. 3, pp. 1569–1580. https://doi.org/10.1104/pp.16.0 0328

  94. Singh, S., Katzer, K., Lambert, J., et al., CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development, Cell Host Microbe, 2014, vol. 15, no. 2, pp. 127–129. https://doi.org/10.1016/j.chom.2014.01.011

    Article  CAS  Google Scholar 

  95. Singh, A., Kumar, A., Yadav, S., and Singh, I.K., Reactive oxygen species-mediated signaling during abiotic stress, Plant Gene, 2019, vol. 18, p. 10017. https://doi.org/10.1016/j.plgene.2019.100173

    Article  CAS  Google Scholar 

  96. Stracke, S., Kistner, C., Yoshida, S., et al., A plant receptor-like kinase required for both fungal and bacterial symbiosis, Nature, 2002, vol. 417, pp. 959–962. https://doi.org/10.1038/nature00841

  97. Suzaki, T., Yoro, E., and Kawaguchi, M., Leguminous plants: inventors of root nodules to accommodate symbiotic bacteria, Int. Rev. Cell Mol. Biol., 2015, vol. 316, pp. 111–158. https://doi.org/10.1016/bs.ircmb.2015.01.004

    Article  CAS  PubMed  Google Scholar 

  98. Tsyganov, V.E. and Tsyganova, A.V., Symbiotic regulatory genes controlling nodule development in Pisum sativum L., Plants, 2020, vol. 9, p. 1741. https://doi.org/10.3390/plants 9121741

  99. Tsygankova, A.V., Tsygankov, V., Borisov, A.Yu., et al., Comparative cytochemical analysis of hydrogen peroxide distribution in pea ineffective mutant SGE-FIX-1 (Sym40) and initial SGE, Ekol. Genet., 2009, vol. 7, no. 3, pp. 1–9.

    Google Scholar 

  100. Tonelli, M.L., Figueredo, M.S., Rodriguez, J., et al., Induced systemic resistance-like responses elicited by rhizobia, Plant Soil, 2020, vol. 448, no. 4, pp. 1–14. https://doi.org/10.1007/s11104-020-04423-5

  101. Tyth, K., Stratil, T.F., Madsen, E.B., et al., Functional domain analysis of the Remorin protein LjSYMREM1 in Lotus japonicas, PLoS One, 2012, vol. 7, no. 1, e30817. https://doi.org/10.1371/journal.pone.0030817

  102. Vasileva, G.G., Glyanko, A.K., Mironova, N.V., and Shmakov, V.N., The content of hydrogen peroxide and catalase activity in sites of pea roots with different sensitivity to infection by nitrogen-fixing bacteria, Visn. Hark. Nac. Agrar. Univ., Ser. Biol., 2007, vol. 1, no. 10, pp. 59–64.

    Google Scholar 

  103. Verni, T., Kim, J., Frances, L., et al., The NIN transcription factor coordinates diverse nodulation programs in different tissues of the Medicago truncatula root, Plant Cell, 2015, vol. 27, no. 12, pp. 3410–3424. https://doi.org/10.1105/tpc.15.00461

  104. Wang, Y., Branicky, R., No, A., and Hekimi, S., Superoxide dismutases: dual roles in controlling ROS damage and regulating ROS signaling, J. Cell Biol., 2018, vol. 217, no. 6, pp. 1915–1928. https://doi.org/10.1083/jcb.201708007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Wang, Q., Liu, J., and Zhu, H., Genetic and molecular mechanisms underlying symbiotic specificity in legume–Rhizobium interactions, Front. Plant Sci., 2018, vol. 9, p. 313. https://doi.org/10.3389/fpls.2018.00313

    Article  PubMed  PubMed Central  Google Scholar 

  106. Wisniewski, J.P., Rathbun, E.A., Knox, J.P., Brewin, N.J., et al., Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: implications for pea nodule initiation by Rhizobium leguminosarum, Mol. Plant–Microbe Interact., 2000, vol. 13, no. 4, pp. 413–420. https://doi.org/10.1094/MPMI.2000.13.4.413

    Article  CAS  PubMed  Google Scholar 

  107. Xue, L., Cui, H., Buer, B., et al., Network of GRAS transcription factors involved in the control of arbuscule development in Lotus japonicus, Plant Physiol., 2015, vol. 167, no. 3, pp. 854–871. https://doi.org/10.1104/pp.114.255430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Yoro, E., Suzaki, T., Toyokura, K., Miyazawa, H., et al., A positive regulator of nodule organogenesis, Nodule Inception, acts as a negative regulator of rhizobial infection in Lotus japonicus, Plant Physiol., 2014, vol. 165, pp. 747–758. https://doi.org/10.1104/pp.113.233379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Yu, S., Kakar, K.U., Yang, Z., et al., Systematic study of the stress-responsive Rboh gene family in Nicotiana tabacum: genome-wide identification, evolution and role in disease resistance, Genomics, 2020, vol. 112, no. 2, pp. 1404–1418. https://doi.org/10.1016/j.ygeno.2019.08.010

    Article  CAS  PubMed  Google Scholar 

  110. Zamioudis, C. and Pieterse, C.M.J., Modulation of host immunity by beneficial microbes, Mol. Plant–Microbe Intract., 2012, vol. 25, pp. 139–150. https://doi.org/10.1094/MPMI-06-11-0179

    Article  CAS  Google Scholar 

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Mamenko, T.P. Regulation of Legume-Rhizobial Symbiosis: Molecular Genetic Aspects and Participation of Reactive Oxygen Species. Cytol. Genet. 55, 447–459 (2021). https://doi.org/10.3103/S0095452721050078

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