Skip to main content
SpringerLink
Log in

Calcium in the Life Cycle of Legume Root Nodules

  • Review article
  • Published:
Indian Journal of Microbiology Aims and scope Submit manuscript

Abstract

The present review highlights both the fundamental questions of calcium localization, compartmentation, and its participation in symbiosome signaling cascades during nodule formation and functioning. Apparently, the main link of such signaling is the calmodulin…calcium- and calmodulin-dependent protein kinases…CYCLOPS…NIN…target genes cascade. The minimum threshold level of calcium as a signaling agent in the presence of intracellular reserves determines the possibility of oligotrophy and ultraoligotrophy in relation to this element. During the functioning of root nodules, the Ca2+-ATPases activity maintains homeostasis of low calcium concentrations in the cytosol of nodule parenchyma cells. Disturbation of this homeostasis can trigger the root nodule senescence. The same reasons determine the increase in the effectiveness of symbiosis with the help of seed priming with sources of calcium. Examples of calcium response polymorphism in components of nitrogen fixing simbiosis important in practical terms are shown.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Guo K, Yang J, Yu N, Luo L, Wang E (2022) Biological nitrogen fixation in cereal crops: progress, strategies, and perspectives. Plant Commun 28:100499. https://doi.org/10.1016/j.xplc.2022.100499

    Article  CAS  Google Scholar 

  2. Granqvist E, Sun J, Op den Camp R et al (2015) Bacterial-induced calcium oscillations are common to nitrogen-fixing associations of nodulating legumes and non-legumes. New Phytol 207:551–558. https://doi.org/10.1111/nph.13464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Leborgne-Castel N, Bouhidel K (2014) Plasme membrane protein trafficking in plant - microbe interactions: a plant cell point of view. Front Plant Sci 5:735. https://doi.org/10.3389/fpls.2014.00735

    Article  Google Scholar 

  4. OʾHara GW, Boonkerd N, Dilworth MJ (1988) Mineral constrains to nitrogen fixation. Plant Soil 108:93–110

    Article  Google Scholar 

  5. González-Guerrero M, Matthiadis A, Saez A, Long TA (2014) Fixating on metals: new insights into the role of metals in nodulation and symbiotic nitrogen fixation. Front Plant Sci 5:1–6. https://doi.org/10.3389/fpls.2014.00045

    Article  Google Scholar 

  6. Gage DJ (2004) Infection and invasion of roots by symbiotic nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 280–300. https://doi.org/10.1128/MMBR.68.2.280-300.2004

  7. Vasil’eva GG, Ischenko AA, Glyan’ko AK (2011) Physiological role of calcium in legume-rhizobium symbiosis. J Stress Physiol Biochem 7:398–414

    Google Scholar 

  8. Weisany W, Raei Y, Allahverdipoor KH (2013) Role of some of mineral nutrients in biological nitrogen fixation. Bull Env Pharmacol Life Sci 2:77–84

    CAS  Google Scholar 

  9. Andreev IM, Andreeva IN, Dubrovo PN, Krylova VV, Kozharinova CM, Izmailov SF (2001) Calcium status of yellow lupin symbiosomes as a potential regulator of their nitrogenase activity: the role of the peribacteroid membrane. Rus J Plant Physiol 48:308–317. https://doi.org/10.1023/A:1016654114889

    Article  CAS  Google Scholar 

  10. Hénault C, Barbier E, Hartmann A, Revellin C (2022) New insights into the use of Rhizobia to mitigate soil N2O emissions. Agriculture 12:271. https://doi.org/10.3390/agriculture12020271

    Article  CAS  Google Scholar 

  11. Yun J, Wang C, Zhang F et al (2023) A nitrogen fixing symbiosis-specific pathway required for legume flowering. Sci. Adv. 9, Art. eade1150. https://doi.org/10.1126/sciadv.ade1150

  12. Chakraborty S, Harris JM (2022) At the crossroads of salinity and rhizobium-legume symbiosis. Mol Plant Microbe Interact 35:540–553. https://doi.org/10.1094/MPMI-09-21-0231-FI

    Article  CAS  PubMed  Google Scholar 

  13. Pei ZM, Gilroy S (2009) Calcium signals and their regulation. Intracellular Signaling in Plants. Edited by Zhenbiao Yang. Ann Plant Rev. 33:137–162. https://doi.org/10.1002/9781444302387

  14. Book chapter Kobayashi H, Broughton WJ (2008) Fine-tuning of symbiotic genes in rhizobia: flavonoid signal transduction cascade. In: Nitrogen-fixing Leguminous Symbioses. Ed by M. J. Dilworth. Springer. 117–152. https://doi.org/10.1007/978-1-4020-3548-7_5

  15. Moscatiello R, Squartini A, Mariani P, Navazio L (2010) Flavonoid-induced calcium signalling in Rhizobium leguminosarum Bv. Viciae. New Phytol 188:814–823. https://doi.org/10.1111/j.1469-8137.2010.03411.x

    Article  CAS  PubMed  Google Scholar 

  16. Moscatiello R, Alberghini S, Squartini A, Mariani P, Navazio L (2009) Evidence for calcium-mediated perception of plant symbiotic signals in aequorin-expressing Mesorhizobium loti. BMC Microbiol. 9, Art. 206. https://doi.org/10.1186/1471-2180-9-206

  17. Book chapter Hassan S, Mathesius U (2015) Flavonoids play multiple roles in symbiotic root-rhizosphere interactions. In: Biological Nitrogen fixation. Ed by Frans J De Bruijn 2501–2509. https://doi.org/10.1002/9781119053095.ch50

  18. Yuan P, Luo F, Gleason C, Poovaiah BW (2022) Calcium_calmodulin-mediated microbial symbiotic interactions in plants. Front. Plant Sci. 13, Art. 984909. https://doi.org/10.3389/fpls.2022.984909

  19. Popp C, Ott T (2011) Regulation of signal transduction and bacterial Infection during root nodule symbiosis. Curr Opin Plant Biol 14:458–467. https://doi.org/10.1016/j.pbi.2011.03.016

    Article  CAS  PubMed  Google Scholar 

  20. Book chapter Stacey G The Rhizobium-legume nitrogen-fixing symbiosis. In: Biology of the Nitrogen Cycle. First edition. Ed.by Bothe H., Ferguson S. J., Newton W. E. Elsevier. 2007. pp. 427. https://doi.org/10.1016/B978-044452857-5.50011-4

  21. Huisman R, Geurts R (2020) A Roadmap toward Engineered Nitrogen-fixing nodule symbiosis. Plant Commun 1–15. https://doi.org/10.1016/j.xplc.2019.100019

  22. Velzena R, Holmera R, Bua F et al (2018) Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses. PNAS. vol. 115. № 20. 470–47009. https://doi.org/10.1073/pnas.1721395115

  23. Book chapter Debnath S, Das N, Maheshwari DK, Pandey P (2022) Interactions of rhizobia with nonleguminous plants: A molecular ecology perspective for enhanced plant growth. In: Nitrogen Fixing Bacteria: Sustainable Growth of Non-legumes. Edited by Maheshwari D. K., Dobhal R., Dheeman S. Springer. 23–64. https://doi.org/10.1007/978-981-19-4906-7

  24. Luan L, Wang C (2021) Calcium Signaling mechanisms across kingdoms. Annu Rev Cell Dev Biol V 37:311–340

    Article  CAS  Google Scholar 

  25. Capoen W, Sun J, Wysham D, Otegui MS, Venkateshwaran M (2011) Nuclear membranes control symbiotic calcium signaling of legumes. PNAS 108:14348–14353. https://doi.org/10.1073/pnas.1107912108

    Article  PubMed  PubMed Central  Google Scholar 

  26. Liu H, Lin J-S, Luo Z et al (2022) Constitutive activation of a nuclear-localized calcium channel complex in Medicago truncatula. PNAS 119:e2205920119. https://doi.org/10.1073/pnas.2205920119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Bredow M, Monaghan J (2022) Cross-kingdom regulation of calcium- and/or calmodulin-dependent protein kinases by phospho-switches that relieve autoinhibition. Curr Opin Plant Biol 68:102251. https://doi.org/10.1016/j.pbi.2022.102251

    Article  CAS  PubMed  Google Scholar 

  28. Jauregui E, Du L, Gleason C, Poovaiah BW (2017) W342F mutation in CCaMK enhances its affinity to calmodulin but compromises its role in supporting root nodule symbiosis in Medicago truncatula. Front Plant Sci 16:1921. https://doi.org/10.3389/fpls.2017.01921

    Article  Google Scholar 

  29. Maunoury N, Kondorosi A, Kondorosi E, Mergaert P (2008) Cell biology of nodule infection and development. Nitrogen-fixing Leguminous Symbioses. Ed by Michael J. Dilworth, Euan K. James, Janet I. Sprent, William E. Newton. Springer. 153–189. https://doi.org/10.1007/978-1-4020-3548-7_6

  30. Book chapter Dupont L, Alloing G, Pierre O et al (2012) The legume root nodule: from symbiotic nitrogen fixation to senescence. In: Senescence. Ed by Dr. Tetsuji Nagata. Publisher in Tech. 137–168. https://doi.org/10.5772/34438

  31. Gong X, Jensen E, Bucerius S, Parniske M (2022) A CCaMK/Cyclops response element in the promoter of Lotus japonicus calcium-binding protein 1 (CBP1) mediates transcriptional activation in root symbioses. New Phytol 235:1196–1211. https://doi.org/10.1111/nph.18112

    Article  CAS  PubMed  Google Scholar 

  32. Akamatsu A, Nagae M, Takeda N (2022) The CYCLOPS response element in the NIN promoter is important but not essential for Infection thread formation during Lotus japonicus–rhizobia symbiosis. MPMI 35:650–658. https://doi.org/10.1094/mpmi-10-21-0252-r

    Article  CAS  PubMed  Google Scholar 

  33. Liu M, Soyano T, Yano K, Hayashi M, Kawaguchi M (2019) ERN1 and CYCLOPS coordinately activate NIN signaling to promote Infection thread formation in Lotus japonicus. J Plant Res 132:641–653. https://doi.org/10.1007/s10265-019-01122-w

    Article  CAS  PubMed  Google Scholar 

  34. Robledo M, Rivera L, Menéndez E et al (2015) Role of Rhizobium cellulase CelC2 in host root colonization and Infection. Biol Nitrogen Fixation Ed Frans J De Bruijn 2525–2531. https://doi.org/10.1002/9781119053095.ch53

  35. Knights HE, Jorrin B, Haskett TL, Poole PS (2021) Deciphering bacterial mechanisms of root colonization. Environ Microbiol Rep 13:428–444. https://doi.org/10.1111/1758-2229.12934

    Article  PubMed  Google Scholar 

  36. Ausmees N, Jacobsson K, Lindberg M (2001) A unipolarly located, cell-surface-associated agglutinin, RapA, belongs to a family of Rhizobium-adhering proteins (rap) in Rhizobium leguminosarum Bv. Trifolii Microbiol 147:549–559. https://doi.org/10.1099/00221287-147-3-549

    Article  CAS  Google Scholar 

  37. Tarsitano J, Ramis LY, Alonso LG, Russo DM, Zorreguieta A (2022) RapD is a multimeric calcium-binding protein that interacts with the Rhizobium leguminosarum biofilm exopolysaccharide, influencing the polymer lengths. Front Microbiol 13:895526. https://doi.org/10.3389/fmicb.2022.895526

    Article  PubMed  PubMed Central  Google Scholar 

  38. Book chapter Sieberer BJ, Fournier J, Timmers ACJ, Chabaud M, Barker DG (2015) Nuclear Ca2+ signaling reveals active bacterial-host communication throughout rhizobial Infection in root hairs of Medicago truncatula. In: Biological Nitrogen fixation. Ed by Frans J De Bruijn 2:567–574. https://doi.org/10.1002/9781119053095.ch57

    Article  Google Scholar 

  39. Liu X, Zhang K, Liu Y, Zou D, Wang D, Xie Z (2020) Effects of calcium and signal sensing systems on Azorhizobium caulinodans biofilm formation and host colonization. Front Microbiol 11:563367. https://doi.org/10.3389/fmicb.2020.563367

    Article  PubMed  PubMed Central  Google Scholar 

  40. Kadreva I, Ignatov G (1995) Role of Ca2+ in Bradyrhizobium japonicum strain 273 attachment ability and accumulation on soybean root surface. J Plant Physiol 145:577–579. https://doi.org/10.1016/S0176-1617(11)81791-8

    Article  Google Scholar 

  41. Tsyganova AV, Brewin NJ, Tsyganov VE (2021) Structure and development of the legume-rhizobial symbiotic interface in infection threads. Cells 10:1050. https://doi.org/10.3390/cells10051050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Vaz Martins T, Livina VN (2019) What drives symbiotic calcium signalling in legumes? Insights and challenges of imaging. Int J Mol Sci 20:2245. https://doi.org/10.3390/ijms20092245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Hayashi T, Shimoda Y, Sato S, Tabata S, Imaizumi-Anraku H, Hayashi M (2014) Rhizobial Infection does not require cortical expression of upstream common symbiosis genes responsible for the induction of Ca2+ spiking. Plant J 77:146–159. https://doi.org/10.1111/tpj.12374

    Article  CAS  PubMed  Google Scholar 

  44. Rival P, Billy F, Bono J-J, Gough C, Rosenberg C, Bensmihen S (2012) Epidermal and cortical roles of NFP and DMI3 in coordinating early steps of nodulation in Medicago truncatula. Dev 139:3383–3391. https://doi.org/10.1242/dev.081620

    Article  CAS  Google Scholar 

  45. Mayhood P, Mirza BS (2021) Soybean root nodule and rhizosphere microbiome: distribution of rhizobial and nonrhizobial endophytes. Appl Environ Microbiol 1–14. https://doi.org/10.1128/AEM.02884-20

  46. Martínez-Hidalgo P, Humm EA, Still DW et al (2022) Medicago root nodule microbiomes: insights into a complex ecosystem with potential candidates for plant growth promotion. PlantSoil 471:507–526. https://doi.org/10.1007/s11104-021-05247-7

    Article  CAS  Google Scholar 

  47. Delgado MJ, Pacheco PJ, Bedmar EJ, Mesa S, Torosa G (2022) Ensifer meliloti denitrification is involved in Infection effectiveness and N2O emissions by alfalfa root nodules. Res Square (Preprint). https://doi.org/10.21203/rs.3.rs-2033464/v1

    Article  Google Scholar 

  48. Woliy K, Degefu T, Frostegård à (2019) Host range and symbiotic effectiveness of N2O reducing Bradyrhizobium strains. Front Microbiol 10:2746. https://doi.org/10.3389/fmicb.2019.02746

    Article  PubMed  PubMed Central  Google Scholar 

  49. Etesami H (2022) Root nodules of legumes: a suitable ecological niche for isolating non-rhizobial bacteria with biotechnological potential in agriculture. Curr Res Biotechnol 4:78–86. https://doi.org/10.1016/j.crbiot.2022.01.003

    Article  CAS  Google Scholar 

  50. Gough C, Cottret L, Lefebvre B, Bono J-J (2018) Evolutionary history of plant LysM receptor proteins related to root endosymbiosis. Front. Plant Sci 9:923. https://doi.org/10.3389/fpls.2018.00923

    Article  Google Scholar 

  51. Scheel D (2013) Calcium and MAP kinase signaling in PAMP-triggered immunity. BioTechnologia 94:353–373

    Google Scholar 

  52. Yu H, Xiao A, Dong R et al (2018) Suppression of innate immunity mediated by the CDPK-Rboh complex is required for rhizobial colonization in Medicago truncatula nodules. New Phytol 220:425–434. https://doi.org/10.1111/nph.15410

    Article  CAS  PubMed  Google Scholar 

  53. Horner GM (1936) Relation of the degree of base saturation of colloidal clay by calcium to the growth, nodulation, and composition of soybeans. Mo Agr Exp Station Res Bul 232:1–36

    Google Scholar 

  54. Greenwood EAN, Hallsworth EG (1960) Studies on the nutrition of forage legumes. II. Some interactions of ca, P, Cu and Mo on the growth and chemical composition of Trifolium subterraneum L. Plant Soil 12:97–127. https://doi.org/10.1007/BF01377365

    Article  CAS  Google Scholar 

  55. Andreeva IN, Kozharinova GM, Izmailov SF (1995) Calcium compartmentation in root nodules of leguminous plants: electron microscope investigation. Dokl Akad Nauk 344:402–406

    CAS  Google Scholar 

  56. Izmailov SF, Andreeva IN, Kozharinova GM (1999) Subcellular calcium localization in the root nodules of legumes. Rus J Plant Physiol 46:93–101

    CAS  Google Scholar 

  57. Izmailov SF (2003) Calcium-based interactions of symbiotic partners in legumes: role of peribacteroid membrane. Rus J Plant Physiol 50:553–566. https://doi.org/10.1023/A:1024789227513

    Article  CAS  Google Scholar 

  58. Ledermann R, Schulte CCM, Poole PS (2021) How rhizobia adapt to the nodule environment. J Bacteriol 203:e0053920. https://doi.org/10.1128/JB.00539-20

    Article  PubMed  Google Scholar 

  59. Tookmanian E, Junghans L, Kulkarni G, Ledermann R, Saenz J, Newman DK (2022) Hopanoids confer robustness to physicochemical variability in the niche of the plant symbiont Bradyrhizobium diazoefficiens. J Bacteriol 204:e0044221. https://doi.org/10.1128/jb.00442-21

    Article  CAS  PubMed  Google Scholar 

  60. Vitiello G, Oliva R, Petraccone L et al (2021) Covalently bonded hopanoid-lipid A from Bradyrhizobium: the role of unusual molecular structure and calcium ions in regulating the lipid bilayers organization. J Colloid Interface Sci 594:891–901. https://doi.org/10.1016/j.jcis.2021.03.072

    Article  CAS  PubMed  Google Scholar 

  61. Santo-Domingo J, Demaurex N (2010) Calcium uptake mechanisms of mitochondria. Biochim Biophys Acta 1797:907–912. https://doi.org/10.1016/j.bbabio.2010.01.005

    Article  CAS  PubMed  Google Scholar 

  62. Book Mitra GN (2015) Regulation of nutrient uptake by plants. New Delhi: Springer 10:978–981. https://doi.org/10.1007/978-81-322-2334-4

    Article  Google Scholar 

  63. Andreev I, Dubrovo P, Krylova V, Izmailov SF (1998) Calcium uptake by symbiosomes and the peribacteroid membrane vesicles isolated from yellow lupin root nodules. J Plant Physiol 153:610–614. https://doi.org/10.1016/S0176-1617(98)80211-3

    Article  CAS  Google Scholar 

  64. Krylova VV, Andreev IM, Andreeva IN, Dubrovo PN, Kozharinova GM, Izmailov SF (2002) Verapamil-sensitive calcium transporter in the peribacteroid membrane of symbiosomes from Vicia faba root nodules. J Plant Physiol 49:746–753. https://doi.org/10.1023/A:1020953326517

    Article  CAS  Google Scholar 

  65. Roberts DM, Tyerman SD (2002) Voltage-dependent cation channels permeable to NH4+, K+, and Ca2+ in the symbiosome membrane of the model legume Lotus japonicus. Plant Physiol 128:370–378. https://doi.org/10.1104/pp.010568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Andreev IM, Dubrovo PN, Krylova VV, Izmailov SF (1999) Functional identification of ATP-driven Ca2+-pump in the peribacteroid membrane of broad bean root nodules. FEBS Lett 49–52. https://doi.org/10.1016/s0014-5793(99)00262-8

  67. Krylova VV, Andreev IM, Zartdinova R, Izmailov SF (2013) Biochemical characterization of Ca2+-ATPase in the peribacteroid membrane of broad bean root nodules. Protoplasma 250:531–538. https://doi.org/10.1007/s00709-012-0436-0

    Article  CAS  PubMed  Google Scholar 

  68. Krylova VV, Zartdinova RF, Andreev IM, Izmailov SF (2016) Ca2+/H+ antiport as a possible mechanism of the Ca2+-translocating ATPase functioning in vesicles of bean root nodule’s symbiosome membrane. Biochem (Moscow) suppl ser A. Membr Cell Biol 10:218–222. https://doi.org/10.1134/S1990747816010074

    Article  Google Scholar 

  69. Krylova VV, Andreev IM, Zartdinova R, Izmailov SF (2017) Ca2+-ATPase in the symbiosome membrane from broad bean root nodules: further evidence for its functioning as ATP-driven Ca2+/H+ exchanger. Acta Physiol Plant 39:247–254. https://doi.org/10.1007/s11738-017-2546-y

    Article  CAS  Google Scholar 

  70. Liu J, Miller SS, Graham M et al (2006) Recruitment of novel calcium-binding proteins for root nodule symbiosis in Medicago truncatula. Plant Physiol 141:167–177. https://doi.org/10.1104/pp.106.076711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Ouyang L-J, Whelan J, Weaver CD, Roberts DM, Day DA (1991) Protein phosphorylation stimulates the rate of malate uptake across the peribacteroid membrane of soybean nodules. FEBS Lett 293:188–190. https://doi.org/10.1016/0014-5793(91)81183-9

    Article  CAS  PubMed  Google Scholar 

  72. Weaver CD, Shomerg NH, Louis CF, Roberts DM (1992) Determination of the site of phosphorylation of nodulin 26 by the calcium-dependent protein kinase from soybean nodules. Biochem 31:8954–8959. https://doi.org/10.1021/bi00152a035

    Article  CAS  Google Scholar 

  73. Zhou S, Zhang C, Huang Y, Chen H, Yuan S, Zhou X (2021) Characteristics and research progress of legume nodule senescence. Plants. https://doi.org/10.3390/plants10061103. 10 1103

    Article  PubMed  PubMed Central  Google Scholar 

  74. Book chapter Kurnet KJ, Foyer CH (2022) Redox metabolism in soybean and its significance in nitrogen – fixing nodules. In: Soybean Physiology and Genetics. Ed by Lam H-M, Li M-W 177–209. https://doi.org/10.1016/bs.abr.2022.02.020

  75. Asad MAU, Zakari SA, Zhao Q, Zhou L, Ye Y, Cheng F (2019) Abiotic stresses intervene with ABA signaling to induce destructive metabolic pathways leading to death: premature leaf senescence in plants. Int J Mol Sci 20:1–23. https://doi.org/10.3390/ijms20020256

    Article  CAS  Google Scholar 

  76. Andreeva IN, Kozharinova GM, Izmailov SF (1998) Senescence of legume nodules. Rus J Plant Physiol 45:101–112

    CAS  Google Scholar 

  77. Nouairi I, Jalali K, Benmoussa S, Kammoun M, Zribi K, Mhadhbi H (2021) CaCl2 seed priming stimulate nodulation and oleosome lipids formation in the root nodules of cadmium-treated faba bean plants. Rhizosphere 18:100326. https://doi.org/10.1016/j.rhisph.2021.100326

    Article  Google Scholar 

  78. Nabi F, Chaker-Haddadj A, Chebaani M, Ghalem A, Mebdoua S, Ounane SM (2020) Influence of seed priming on early stages growth of cowpea [Vigna unguiculata (l.) walp.] Grown under salt stress conditions. Legume Res 43:665–671. https://doi.org/10.18805/LR-504

    Article  Google Scholar 

Download references

Funding

This work supported by government task 1220427000439. The authors collaborated on all stages of preparation of this manuscript.

Author information

Authors and Affiliations

  1. Nitrogen Exchange Laboratory, Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Moscow, Russia

    Rozaliya Zartdinova & Andrey Nikitin

Authors
  1. Rozaliya Zartdinova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrey Nikitin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rozaliya Zartdinova.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zartdinova, R., Nikitin, A. Calcium in the Life Cycle of Legume Root Nodules. Indian J Microbiol 63, 410–420 (2023). https://doi.org/10.1007/s12088-023-01107-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12088-023-01107-3

Keywords

Search

Navigation