Skip to main content
Log in

Calcium-Based Interactions of Symbiotic Partners in Legumes: Role of Peribacteroid Membrane

  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Based on experimental evidence, a concept is formulated that mutualistic relationships between pro- and eukaryotic cells during nitrogen-fixing legume–rhizobia symbiosis rely both on selective transfer of metabolites and ion transport, Ca2+ in particular, across the peribacteroid membrane (PBM). PBM in the nitrogen-fixing cells of yellow lupine (Lupinus luteus L.) and broad bean (Vicia faba L.) is endowed with a calcium-translocating ATPase that pumps Ca2+ into the symbiosome. This pumping ensures, on the one hand, calcium homeostasis in the cytosol of infected plant cells and, on the other hand, it optimizes Ca2+ level in symbiosomes, first of all in the bacteroids, because Ca2+ is one of the main factors controlling their nitrogenase activity. The balance between the symbiotic partners and the maintenance of optimal Ca2+ level in the bacteroids also depends on passive Ca2+ efflux from symbiosomes to the plant cell cytosol via calcium channels. The Ca2+-transporting mechanisms residing at PBM are characterized.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  1. Izmailov, S.F., Physiology of Symbiotic Relations in Legume Nodules: Biosynthesis and Functions of Peribacteroid Membranes, Fiziol. Rast. (Moscow), 1996, vol. 43, pp. 773–791 (Russ. J. Plant Physiol., Engl. Transl.).

    Google Scholar 

  2. Udvardi, M.K. and Day, D.A., Metabolite Transport across the Peribacteroid Membrane from Soybean Root Nodules, Plant Physiol., 1989, vol. 90, pp. 982–987.

    Google Scholar 

  3. Herrada, G., Puppo, A., and Rigaud, J., Uptake of Metabolites by Bacteroid-Containing Vesicles and by Free Bacteroids from French Bean Nodules, J. Gen. Microbiol., 1989, vol. 135, pp. 3165–3171.

    Google Scholar 

  4. Rosendahl, L., Dilworht, M.J., and Glenn, A.R., Exchange of Metabolites across the Peribacteroid Membrane in Pea Root Nodules, J. Plant Physiol., 1992, vol. 139, pp. 635–638.

    Google Scholar 

  5. Radyukina, N.L., Bruskova, R.K., and Izmailov, S.F., The Transport of 14C-Substrates across the Peribacteroid Membrane of Yellow Lupin Nodules, Dokl. Akad. Nauk, 1992, vol. 323, pp. 603–606.

    Google Scholar 

  6. Udvardi, M.K. and Day, D.A., Metabolite Transport across Symbiotic Membranes of Legume Nodules, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1997, vol. 48, pp. 493–523.

    Google Scholar 

  7. Blevins, D.G., Barnett, N.M., and Bottino, P.J., The Effects of Calcium and Ionophore A23187 on Nodulation, Nitrogen Fixation and Growth of Soybean, Physiol. Plant., 1977, vol. 41, pp. 235–238.

    Google Scholar 

  8. Miller, R.W. and Sirois, J.C., Calcium and Magnesium Effects on Symbiotic Nitrogen Fixation in the Alfalfa (Midicago sativa)-Rhizobium meliloti System, Physiol. Plant., 1983, vol. 58, pp. 464–470.

    Google Scholar 

  9. Smit, G., Logman, T.J.J., Boerrigter, M.E., Kijne, J.W., and Lugtenberg, B.J.J., Purification and Partial Characterization of the Rhizobium leguminosarum biovar viciae Ca2+-Dependent Adhesin, which Mediates the First Step in Attachment of Cells of the Family Rhizobiaceae to Plant Root Hair Tips, J. Bacteriol., 1989, vol. 171, pp. 4054–4062.

    Google Scholar 

  10. Lowther, W.L. and Loneragan, J.F., Calcium and Nodulation in Subterranean Clover (Trifolium subterraneum L.), Plant Physiol., 1968, vol. 43, pp. 1362–1366.

    Google Scholar 

  11. Streeter, J.G., Effect of Elevated Calcium Concentration in Infected Cells of Soybean (Glycine max (L.). Merr) Nodules on Nitrogenase Activity and N Input to the Plant, J. Exp. Bot., 1998, vol. 49, pp. 997–1003.

    Google Scholar 

  12. Izmailov, S.F., Andreeva, I.N., and Kozharinova, G.M., Subcellular Calcium Localization in the Root Nodules of Legumes, Fiziol. Rast. (Moscow), 1999, vol. 46, pp. 109–118 (Russ. J. Plant Physiol., Engl. Transl.).

    Google Scholar 

  13. Marme, D., The Role of Calcium in the Regulation of Plant Metabolism, Molecular and Cellular Aspects of Calcium in Plant Development, Trewavas, A.J., Ed., New York: Plenum, 1985, vol. 104, pp. 1–8.

    Google Scholar 

  14. Andreeva, I.N., Andreev, I.M., Dubrovo, P.N., Kozharinova, G.M., Krylova, V.V., and Izmailov, S.F., Calcium Stores in Symbiosomes from Yellow Lupin Root Nodules, J. Plant Physiol., 1999, vol. 155, pp. 357–363.

    Google Scholar 

  15. Andreev, I.M., Andreeva, I.N., Kozharinova, G.M., Dubrovo, P.N., Krylova, V.V., and Izmailov, S.F., Accumulation of Calcium and Its Involvement in the Control of Nitrogenase Activity in the Symbiosomes of Broad Bean Root Nodules, Fiziol. Rast. (Moscow), 2000, vol. 47, pp. 14–20 (Russ. J. Plant Physiol., Engl. Transl.).

    Google Scholar 

  16. Andreev, I.M., Andreeva, I.N., Dubrovo, P.N., Krylova, V.V., Kozharinova, G.M., and Izmailov, S.F., Calcium Status in Yellow Lupin Symbiosomes as a Potential Regulator of Their Nitrogenase Activity: The Role of Peribacteroid Membrane, Fiziol. Rast. (Moscow), 2001, vol. 48, pp. 364–374 (Russ. J. Plant Physiol., Engl. Transl.).

    Google Scholar 

  17. Krylova, V.V., Andreev, I.M., Andreeva, I.N., Dubrovo, P.N., Kozharinova, G.M., and Izmailov, S.F., Verapamil-Sensitive Calcium Transporter in the Peribacteroid Membrane of Symbiosomes from Vicia faba L. Root Nodules, Fiziol. Rast. (Moscow), 2002, vol. 49, pp. 839–846 (Russ. J. Plant Physiol., Engl. Transl.).

    Google Scholar 

  18. Andreev, I.M., Dubrovo, P.N., Krylova, V.V., and Izmailov, S.F., Functional Identification of ATP-Driven Ca2+ Pump in the Peribacteroid Membrane of Broad Bean Root Nodules, FEBS Lett., 1999, vol. 447, pp. 49–52.

    Google Scholar 

  19. Andreev, I.M., Dubrovo, P.N., Krylova, V.V., and Izmailov, S.F., Calcium Uptake by Symbiosomes and the Peribacteroid Membrane Vesicles Isolated from Yellow Lupin Root Nodules, J. Plant Physiol., 1998, vol. 153, pp. 610–614.

    Google Scholar 

  20. Dubrovo, P.N., Krylova, V.V., Livanova, G.I., Zhiznevskaya, G.Ya., and Izmailov, S.F., The Properties of ATPase from the Peribacteroid Membrane of Yellow Lupin Root Nodules, Fiziol. Rast. (Moscow), 1992, vol. 39, pp. 96–108 (Sov. Plant Physiol., Engl. Transl.).

    Google Scholar 

  21. Andreev, I.M., Dubrovo, P.N., Koren'kov, V.D., Krylova, V.V., Sorokin, E.M., and Izmailov, S.F., ATP-Dependent Electrogenic Proton Transport and Translocation of Metabolites across the Peribacteroid Membrane of Lupin, Fiziol. Rast. (Moscow), 1996, vol. 43, pp. 874–882 (Russ. J. Plant Physiol., Engl. Transl.).

    Google Scholar 

  22. White, P.J., Calcium Channels in Higher Plants, Biochim. Biophys. Acta, 2000, vol. 1465, pp. 171–189.

    Google Scholar 

  23. Fedorova, E.E., Al'dzhaparova, Zh.K., Zhiznevskaya, G.Ya., and Izmailov, S.F., Phytohormones in Nitrogen-Fixing Nodules of Legumes, Fiziol. Biokhim. Kul't. Rast., 1991, vol. 23, pp. 426–437.

    Google Scholar 

  24. Fedorova, E.E., Al'dzhaparova, Zh.K., Zhiznevskaya, G.Ya., Artemenko, E.N., and Izmailov, S.F., Phytohormones in Root Nodules of Soybean Plants, Fiziol. Rast. (Moscow), 1992, vol. 39, pp. 224–230 (Sov. Plant Physiol., Engl. Transl.).

    Google Scholar 

  25. Weaver, C.D., Crombie, B., Stacey, G., and Roberts, D.M., Calcium-Dependent Phosphorylation of Symbiosome Membrane Proteins from Nitrogen-Fixing Soybean Nodules, Plant Physiol., 1991, vol. 95, pp. 222–227.

    Google Scholar 

  26. Ou Yang, L.-J., Whelan, J., Weaver, C.D., Roberts, D.M., and Day, D.A., Protein Phosphorylation Stimulates the Rate of Malate Uptake across the Peribacteroid Membrane of Soybean Nodules, FEBS Lett., 1991, vol. 293, pp. 188–190.

    Google Scholar 

  27. Weaver, C.D. and Roberts, D.M., Determination of the Site of Phosphorylation of Nodulin 26 by the Calcium-Dependent Protein Kinase from Soybean Nodules, Biochemistry, 1992, vol. 31, pp. 8954–8959.

    Google Scholar 

  28. Andreev, I., Dubrovo, P., Krylova, V., Andreeva, I., Koren'kov, V., Sorokin, E., and Izmailov, S., Characterization of ATP-Hydrolyzing and ATP-Driven Proton-Translocating Activities Associated with the Peribacteroid Membrane from Root Nodules of Lupinus luteus L., J. Plant Physiol., 1997, vol. 151, pp. 563–569.

    Google Scholar 

  29. Tyerman, S.D., Whitehead, L.F., and Day, D.A., A Channel-Like Transporter for on the Symbiotic Interface of N2-Fixing Plants, Nature, 1995, vol. 378, pp. 629–632.

    Google Scholar 

  30. Whitehead, L.F., Day, D.A., and Tyerman, S.D., Divalent Cation Gating of an Ammonium Permeable Channel in the Symbiotic Membrane from Soybean Nodules, Plant J., 1998, vol. 16, pp. 313–324.

    Google Scholar 

  31. Margulis, L., Symbiosis in Cell Evolution. Life and Its Environment on the Early Earth, San Francisco: Freeman, 1981. Translated under the title Rol' simbioza v evolyutsii kletki, Moscow: Mir, 1983.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Izmailov, S.F. Calcium-Based Interactions of Symbiotic Partners in Legumes: Role of Peribacteroid Membrane. Russian Journal of Plant Physiology 50, 553–566 (2003). https://doi.org/10.1023/A:1024789227513

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1024789227513

Navigation