Abstract
Certain aspects of Ca-dependent regulation of symbiosomes functioning mediated by the operation of Ca2+-translocating ATPase on the symbiosome membrane (SM) were considered. As follows from the results recently obtained by us, the mechanism underlying the action of this calcium pump exhibits a certain functional feature caused by that transfer by it of calcium ion through the SM is closely coupled with transmembrane translocation through the same membrane but in opposite direction of H+ ions. The data here outlined show that such the cation-exchanged mechanism of the Ca2+-ATPase operation can putatively lead to corresponding modulation or maintenance of both ionic and redox homeostasis of the symbiosome space (SS) around bacteroids at a proper level and thereby to the regulation of symbiosomes functioning. It is suggested that based on the same mechanism inherent function of the enzyme in question is associated with its involvement in symbiotic partner cells signaling as well. All these potential activities of the Ca2+-ATPase lead to the important question whether it is the factor determining substantial functions of symbiosomes. Although it is evident that research an answer to this question is a complex enough experimental problem, its solution may give significant contribution to elucidating mechanisms of Ca-dependent regulation of the processes occurring in mature symbiosomes.
Similar content being viewed by others
REFERENCES
Plieth, C., Calcium: just another regulator in the machinery of life? Ann. Bot., 2005, vol. 96, pp. 1–8.
Kleist, T.J. and Luan, S., Constant change: dynamic regulation of membrane transport by calcium signaling networks keeps plants in tune with their environment, Plant Cell Environ., 2016, vol. 39, pp. 467–481.
Andreev, I.M., Emerging evidence for potential role of Ca2+-ATPase-mediated calcium accumulation in symbiosomes of infected root nodule cells, Funct. Plant Biol., 2017, vol. 44, pp. 955–960.
Udvardi, M.K. and Day, D.A., Metabolite transport across symbiotic membranes of legume nodules, Annu. Rev. Plant Physiol., 1997, vol. 48, pp. 493–523.
Andreev, I.M., Dubrovo, P.N., Krylova, V.V., Andreeva, I.N., Korenkov, V.D., Sorokin, E.M., and Izmailov, S.F., Characterization of ATP-hydrolizing and ATP-driven proton-translocating activities associated with the peribacteroid membrane of Lupinus luteus L., J. Plant Physiol., 1997, vol. 151, pp. 563–569.
Andreev, I.M., Dubrovo, P.N., Krylova, V.V., and Izmailov, S.F., Calcium uptake by symbiosomes and the peribacteroid vesicles isolated from yellow lupin root nodules, J. Plant Physiol., 1998, vol. 151, pp. 203–211.
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.
Pierre, O., Engler, G., Hopkins, J., Brau, F., Boncompagni, E., and Herouart, D., Peribacteroid space acidification: a marker of mature bacteroid functioning in Medicago truncatula nodules, Plant Cell Environ., 2013, vol. 36, pp. 2059–2070.
Matamoros, M.A., Dalton, D.A., Ramos, J., Clemente, M.R., Rubio, M.C., and Becana, M., Biochemistry and molecular biology of antioxidants in the rhizobia-legume symbiosis, Plant Physiol., 2003, vol. 133, pp. 499–509.
De la Peña, T.C., Fedorova, E., Pueyo, J.J., and Lucas, M.M., The symbiosome: legume and rhizobia co-evolution toward a nitrogen-fixing organelle? Front. Plant Sci., 2017, vol. 8: 2229. https://doi.org/10.3389/fpls.2017.02229
Gazarini, M.L., Thomas, A.P., Pozzan, T., and Garcia, C.R.S., Calcium signaling in a low calcium environment; how the intracellular malaria parasite solves the problem, J. Cell Biol., 2003, vol. 161, pp. 103–110.
Kazmierczak, J., Kempe, S., and Kremer, B., C-alcium in the early evolution of living systems: bi-ohistorical approach, Curr. Org. Chem., 2013, vol. 17, pp. 1738–1750.
Andreev, I.M., Functions of the vacuole in higher plant cells, Russ. J. Plant Physiol., 2001, vol. 48, pp. 672–680.
Krylova, V.V., Andreev, I.M., Zartdinova, R.F., and Izmailov, S.F., Biochemical characteristics of the Ca2+ pumping ATPase in the peribacteroid membrane from broad bean root nodules, Protoplasma, 2013, vol. 250, pp. 531–538.
Krylova, V.V., Andreev, I.M., Zartdinova, R.F., and Izmailov, S.F., 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., 2017, vol. 39, pp. 247–254.
Holton, M.L., Wang, W., Emerson, M., Neyses, L., and Armesilla, A.L., Plasma membrane calcium ATPases as novel regulators of signal transduction pathways, World J. Biol. Chem., 2010, vol. 1, pp. 201–208.
Strehler, E.E., Caride, A.J., Filoteo, A.G., Xiong, Y., Penniston, J.T., and Enyedi, A., Plasma membrane Ca2+-ATPases as dynamic regulators of cellular calcium handling, Ann. N.Y. Sci., 2007, vol. 1099, pp. 226–236.
Jones, H.E., Holland, I.B., and Campbell, A.K., Direct measurements of free Ca2+ shows different regulation of Ca2+ between the periplasm and cytosol of Escherichia coli, Cell Calcium, 2002, vol. 32, pp. 183–192.
Dominguez, D.C., Guragain, M., and Patrauchan, M., Calcium binding proteins and calcium signaling in prokaryotes, Cell Calcium, 2015, vol. 57, pp. 151–165.
Plattner, H. and Verkhratsky, A., The ancient roots of calcium signaling evolutionary tree, Cell Calcium, 2015, vol. 57, pp. 123–132.
Preisig, O., Zufferrey, R., Thony-Meyer, L., Appleby, C.A., and Henneke, H., A high-affinity cbb 3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum, J. Bacteriol.,1996, vol. 178, pp. 1532–1538.
Poovaiah, B.W. and Du, L., Calcium signaling: decoding mechanism of calcium signatures, New Phytol., 2018, vol. 217, pp. 1598–1609.
De Marco, S.J., Chika, M.C., and Strehler, E.E., Plasma membrane Ca2+-ATPase isoform 2b interacts with Na+/H+ exchanger regulator factor 2 in apical plasma membranes, J. Biol. Chem., 2002, vol. 277, pp. 10506–10511.
Obara, K., Miyashima, N., Xu, C., Toyashima, I., Sugita, Y., Inesi, G., and Toyashima, C., Structural role of countertransport in Ca2+ pump crystal structure in the absence of Ca2+, Proc. Natl. Acad. Sci. USA, 2005, vol. 102, pp. 14489–14496.
Thomas, R.C., The plasma membrane calcium ATPase (PMCA) of neurons is electroneutral and exchanges 2H+ for each Ca2+ or Ba2+ ion extruded, J. Physiol., 2009, vol. 587, pp. 315–327.
Krylova, V.V., Zartdinova, R.F., Andreev, I.M., and Izmailov, S.F., Ca2+/H+ antiport as a possible mechanism of the Ca2+-translocating ATPase functioning in vesicles of bean root nodule symbiosome membrane, Biochemistry (Moscow), Suppl. Ser. A: Membr. Cell Biol., 2016, vol. 10, pp. 218–222.
Valentine, J.S. and Curtis, A.B., A convenient preparation of solutions of superoxide anion and the reaction of superoxide anion with copper complex, J. Am. Chem. Soc., 1975, vol. 97, pp. 224–226.
Chang, C., Damiani, I., Puppo, A., and Frendo, P., Redox changes during the legume-rhizobium symbiosis, Mol. Plant, 2009, vol. 2, pp. 370–377.
Chen, X., Bao, H., Guo, J., Jia, W., Tai, F., Nie, L., Jiang, P., Feng, Y., Lv, S., and Li, Y., Na+/H+ exchanger 1 participates in tobacco disease against Phytophthora parasitica var. nicotianae by affecting vacuolar pH and priming the antioxidant system, J. Exp. Bot., 2014, vol. 65, pp. 6107–6112.
Ahmadi, H., Corsa, M., Weber, M., Verbruggen, N., and Clemens, S., CAX1 suppresses Cd-induced generation of reactive oxygen species in Arabidopsis halleri, Plant Cell Environ., 2018, vol. 41, pp. 2435–2448.
Jones, K.M., Kobayashi, M., Davies, B.W., Taga, M.E., and Walker, G.C., How rhizobial symbiont invade plants: the Sinorhizobium–Medicago model, Nat. Rev. Microbiol., 2007, vol. 5, pp. 619–633.
Behera, S., Zhaolong, X., Luoni, L., Bonza, M.C., Doculla, F.G., de Michelis, M.I., Morris, R.J., Schwarzlander, M., and Costa, A., Cellular Ca2+ signals generate defined pH signatures in plants, Plant Cell, 2018, vol. 30, pp. 2704–2719. https://doi.org/10.1105/tpc.18.00655
Author information
Authors and Affiliations
Contributions
Andreev I.M. wrote the article, while Krylova V.V. prepared the figure for it and participated in discussion of a number of issues raised in the present work.
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 as objects of research.
Additional information
Abbreviations: BM—bacteroid membrane; SM—symbiosome membrane; SOD—superoxide dismutase; SS—symbiosome space.
Rights and permissions
About this article
Cite this article
Andreev, I.M., Krylova, V.V. The Ca2+-ATPase in Legume Root Nodule Peribacteroid Membrane as a Potential Key Determinant of Ca-Dependent Regulation of Symbiosome Functioning. Russ J Plant Physiol 66, 673–678 (2019). https://doi.org/10.1134/S1021443719050030
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1021443719050030