Metabolite transport across the peribacteroid membrane during broad bean development

Pleiades Publishing Ltd - Tập 54 - Trang 184-190 - 2007
V. V. Krylova1, P. N. Dubrovo1, S. F. Izmailov1
1Timiryazev Institute of Plant Physiology Russian Academy of Sciences, Moscow, Russia

Tóm tắt

A temporal pattern of the peribacteroid membrane (PBM) transport function was studied. Spectrophotometric recording was used for establishing the effect of carbon-and nitrogen-containing substrates (malate, succinate, and glutamate) on the acidification of the peribacteroid space and the intensity of light scattering in the symbiosome suspension from broad bean (Vicia faba L.) root nodules of different age. At the early stages of nodule formation and functioning, PBM is permeable not only for malate and succinate, but also for glutamate, and this permeability fully provides for the active bacteroid division and the nitrogenase complex synthesis in the bacteroids at the expense of the carbon-and nitrogen-containing substrates. Mature nodules are characterized by the greatest nitrogen-fixing activity. In these nodules, PBM is selectively permeable for malate and succinate, but constitutes a barrier for glutamate. Thereby, mutually beneficial relations between the symbiotic partners are achieved. In senescent nodules, a rearrangement of symbiotic interactions is directed toward a minimization of both carbon and nitrogen metabolite consumption by the bacteroids. It is concluded that, in the course of the development of the legume-rhizobia symbiosis, the PBM transport function is changed. This function determines a qualitatively different pattern of symbiotic partner interactions in the following sequence: parasitism-mutualism-commensalism.

Tài liệu tham khảo

Izmailov, S.F., Physiology of Symbiotic Relations in Legume Nodules: Biogenesis and Functions of the Peribacteroid Membrane, Russ. J. Plant Physiol., 1996, vol. 43, pp. 672–687. 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. Parniske, M., Intracellular Accommodation of Microbes by Plants: A Common Developmental Program for Symbiosis and Disease? Curr. Opin. Plant Biol., 2000, vol. 3, pp. 320–328. Whitehead, L.F. and Day, D.A., The Peribacteroid Membrane, Physiol. Plant., 1997, vol. 100, pp. 30–44. Lodwig, E. and Poole, P., Metabolism of Rhyzobium Bacteroids, Crit. Rev. Plant Sci., 2003, vol. 22, pp. 37–78. Izmailov, S.F., Calcium-Based Interactions of Symbiotic Partners in Legumes: Role of Peribacteroid Membrane, Russ. J. Plant Physiol., 2003, vol. 50, pp. 553–566. Rin’kis, G.Ya., Optimizatsiya mineral’nogo pitaniya rastenii (Optimization of Plant Mineral Nutrition), Riga: Zinatne, 1972. Andreeva, I.N., Svaradzh, K., Chetverikov, A.G., and Kozlova, G.I., Changes of the Ultrastructure, Nitrogen Fixation Activity of Root Nodules, and the Photosynthetic Apparatus in Soybean during Prolonged Darkness, Fiziol. Rast. (Moscow), 1986, vol. 33, pp. 252–263 (Sov. Plant Physiol., Engl. Transl.). Andreev, I., Dubrovo, P., Krylova, V., Andreeva, I., 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. Palmgren, M.G., Acridine Orange as a Probe for Measuring pH Gradients across Membranes: Mechanism and Limitations, Anal. Biochem., 1991, vol. 192, pp. 316–321. Appel, H.-J. and Bersh, B., Oxonol VI as an Optical Indicator for Membrane Potentials in Lipid Vesicles, Biochim. Biophys. Acta, 1987, vol. 903, pp. 480–494. Dubrovo, P.N., Krylova, V.V., Livanova, G.I., Zhiznevskaya, G.Ya., and Izmailov, S.F., Properties of ATPases of the Peribacteroid Membrane from Root Nodules of Lupinus luteus, Fiziol. Rast. (Moscow), 1992, vol. 39, pp. 503–513 (Sov. Plant Physiol., Engl. Transl.). Rosendahl, L., Dilworth, 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. Bradford, M.M., Rapid and Sensitive Method for Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding, Anal. Biochem., 1976, vol. 72, pp. 248–254. Provorov, N.A., Theory of Symbiosis: Basics of Evolutionary Genetics, Zh. Obshch. Biol., 2001, vol. 62, pp. 472–495. Puppo, A., Groten, K., Bastian, F., Carzaniga, R., Soussi, M., Lucas, M., Felipe, M., Harrison, J., Vanacker, H., and Foyer, C., Legume Nodule Senescence: Roles for Redox and Hormone Signaling in the Orchestration of the Natural Aging Process, New Phytol., 2005, vol. 165, pp. 683–701. Coruzzi, G. and Zhou, L., Carbon and Nitrogen Sensing and Signaling in Plants: Emerging ‘Matrix Effects,’ Curr. Opin. Plant Biol., 2001, vol. 4, pp. 247–253. Demidchik, V., Essah, P., and Tester, M., Glutamate Activates Cation Currents in the Plasma Membrane of Arabidopsis Root Cells, Planta, 2004, vol. 219, pp. 167–175. Day, D.A., Poole, P.S., Tyerman, S.D., and Rosendahl, L., Ammonia and Amino Acid Transport across Symbiotic Membranes in Nitrogen-Fixing Legume Nodules, Cell Mol. Life Sci., 2001, vol. 58, pp. 61–71. Ouyang, L., 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. Mulder, L., Hogg, B., Bersoult, A., and Cullimore, J., Integration of Signalling Pathways in the Establishment of the Legume-Rhizobia Symbiosis, Physiol. Plant., 2005, vol. 123, pp. 207–218. Peoples, M.B. and Dalling, M.J., The Interplay between Proteolysis and Amino Acid Metabolism during Senescence and Nitrogen Reallocation, Senescence and Aging in Plants, Nooden, L.D. and Leopold, A.C., Eds., New York: Academic, 1988, pp. 181–217. Brewin, N.J., Development of the Legume Root Nodule, Annu. Rev. Cell Biol., 1991, vol. 7, pp. 191–226. Mellor, R.B., Bacteroids in the Rhizobium-Legume Symbiosis Inhabit a Plant Internal Lytic Compartment: Implications for Other Microbial Endosymbiosis, J. Exp. Bot., 1989, vol. 40, pp. 831–839. Andreeva, I.N., Kozharinova, G.M., and Izmailov, S.F., Senescence of Legume Nodules, Russ. J. Plant Physiol., 1998, vol. 45, pp. 101–112.