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.
Similar content being viewed by others
REFERENCES
Andrio, E., Marino, D., Marmeys, A., et al., Hydrogen peroxide-regulated genes in the Medicago truncatula–Sinorhizobium meliloti symbiosis, New Phytol., 2013, vol. 198, no. 1, pp. 179–189. https://doi.org/10.1111/nph.12120
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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.
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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 max–Bradyrhizobium japonicum under drought conditions, Mikrobiol. Z., 2019, vol. 81, no. 4, pp. 65–72. https://doi.org/10.15407/microbiolj81.04.062
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
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
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
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
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
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
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
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
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
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
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
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
Mamenko, T.P., Khomenko, Yu.O., and Kots, S.Ya., Activity of superoxide dismutase and enzymes of ascorbate-glutathione cycle in Glycine max–Bradyrhizobium japonicum symbiotic systems with action drought, Mikrobiol. Z., 2018, vol. 80, no. 3, pp. 77–88. https://doi.org/10.15407/microbiolj80.03.077
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
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
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
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
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
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
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
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
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
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
Morgun, V.V., Kots, S.Ya., Mamenko, T.P., and Vorobey, N.A., Lipid peroxidation intensity in different on effectiveness of symbiotic systems Glycine max–Bradyrhizobium japonicum under drought conditions, Mikrobiol. Z., 2020, vol. 82, no. 4, pp. 23–30. https://doi.org/10.15407/microbi-olj82.04.023
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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.
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
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
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.
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
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
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
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
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
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
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
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
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.
Additional information
Translated by V. Mittova
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.3103/S0095452721050078