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Specificity and regulation of the dicarboxylate carrier on the peribacteroid membrane of soybean nodules

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Abstract

Malate and succinate were taken up rapidly by isolated, intact peribacteroid units (PBUs) from soybean (Glycine max (L.) Merr.) root nodules and inhibited each other in a competitive manner. Malonate uptake was slower and was severely inhibited by equimolar malate in the reaction medium. The apparent Km for malonate uptake was higher than that for malate and succinate uptake. Malate uptake by PBUs was inhibited by (in diminishing order of severity) oxaloacetate, fumarate, succinate, phthalonate and oxoglutarate. Malonate and butylmalonate inhibited only slightly and pyruvate,isocitrate and glutamate not at all. Of these compounds, only oxaloacetate, fumarate and succinate inhibited malate uptake by free bacteroids. Malate uptake by PBUs was inhibited severely by the uncoupler carbonylcyanidem-chlorophenyl hydrazone and the respiratory poison KCN, and was stimulated by ATP. We conclude that the peribacteroid membrane contains a dicarboxylate transport system which is distinct from that on the bacteroid membrane and other plant membranes. This system can catalyse the rapid uptake of a range of dicarboxylates into PBUs, with malate and succinate preferred substrates, and is likely to play an important role in symbiotic nitrogen fixation. Energization of both the bacteroid and peribacteroid membranes controls the rate of dicarboxylate transport into peribacteroid units.

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Abbreviations

CCCP:

carbonylcyanidem-chlorophenyl hydrazone

Dct:

dicarboxylate transport

PBM:

peribacteroid membrane

PBU:

peribacteroid unit

References

  • Appley, C.A. (1984) Leghemoglobin andRhizobium respiration. Annu. Rev. Plant Physiol.35, 443–478

    Article  Google Scholar 

  • Blumwald, E., Fortin, M.G., Rea, P.A., Verma D.P.S., Poole, R.J. (1985) Presence of host-plasmamembrane type H+-ATPase in the membrane envelope enclosing the bacteroids in soybean root nodules. Plant Physiol.78, 655–672

    Google Scholar 

  • Day, D.A., Wiskich, J.T. (1984) Transport processes of isolated plant mitochondria. Physiol. Vég.22, 241–261

    CAS  Google Scholar 

  • Day, D.A., Price, G.D., Gresshoff, P.M. (1986) Isolation and oxidative properties of mitochondria and bacteroids from soybean root nodules. Protoplasma134, 121–129

    Article  CAS  Google Scholar 

  • Day, D.A., Price, G.D., Udvardi, M.K. (1989) The membrane interface of theBradyrhizobium japonicum-Glycine max symbiosis: peribacteroid units from soybean nodules. Aust. J. Plant Physiol.16, 69–84

    Article  CAS  Google Scholar 

  • Dilworth, M., Glenn, A. (1984) How does a legume nodule work? Trends Biochem. Sci.9, 519–523

    Article  CAS  Google Scholar 

  • Domigan, N.M., Farnden, K.J.F., Robertson, J.G., Monk, B.C. (1988) Characterization of the peribacteroid membrane ATPase of lupin root nodules. Arch. Biochem. Biophys.264, 564–573

    Article  PubMed  CAS  Google Scholar 

  • Flügge, I.U., Woo, K.C., Heldt, H.W. (1988) Characteristics of 2-oxoglutarate and glutamate transport in spinach chloroplasts. Planta174, 534–541

    Article  Google Scholar 

  • Heldt, H., Flügge, U.I. (1987) Subcellular transport of metabolites in plant cells. In: The biochemistry of plants, vol. 12, pp. 49–85, Davies, D.D., ed. Academic Press, New York

    Google Scholar 

  • Herrada, G., Puppo, A., Rigaud, J. (1989) Uptake of metabolites by bacteroid-containing vesicles and by free bacteroids from french bean nodules. J. Gen. Microbiol.135, 3165–3171

    CAS  Google Scholar 

  • Humbeck, C., Werner, D. (1987) Separation of malate and malonate pools by the peribacteroid membrane in soybean nodules. Endocyt. Cell Res.4, 185–196

    Google Scholar 

  • Lüttge, U., Ball, E. (1979) Electrochemical investigation of active malic acid transport at the tonoplast into the vacuoles of the CAM plantKalanchöe daigremontiana. J. Membr. Biol.47, 401–422

    Article  Google Scholar 

  • Marigo, G., Bonyssou, H., Laborie, D. (1988) Evidence for a malate transport into vacuoles isolated fromCatharanthus roseus cells. Bot Acta101, 187–191

    CAS  Google Scholar 

  • Martinoia, E., Flügge, U.I., Kaiser, G., Heber, U., Heldt, H.W. (1985) Energy-dependent uptake of malate into vacuoles isolated from barley mesophyll-protoplasts. Biochim. Biophys. Acta806, 311–319

    Article  CAS  Google Scholar 

  • McKay, I.A., Dilworth, M.J., Glenn, A.R. (1988) C4-dicarboxylate metabolism in free-living and bacteroid forms ofRhizobium leguminosarum MNF3481. J. Gen. Microbiol.134, 1433–1440

    CAS  Google Scholar 

  • Mellor, R.B. (1989) Bacteroids in theRhizobium-legume symbiosis inhabit a plant internal lytic compartment: implications for other microbial endosymbioses. J. Exp. Bot.40, 831–839

    CAS  Google Scholar 

  • Mellor, R.B., Werner, D. (1987) Peribacteroid membrane biogenesis in mature legume root nodules. Symbiosis3, 75–100

    CAS  Google Scholar 

  • Minchin, F.R., Sheehey, J.E., Minguez, M.I., Whitty, J.F. (1985) Characterization of the resistance to oxygen diffusion in legume nodules. Ann. Bot.55, 53–60

    Google Scholar 

  • Palmieri, F., Klingenberg, M. (1979) Direct method for measuring metabolite transport and distribution in mitochondria. Methods Enzymol.56, 279–301

    Article  PubMed  CAS  Google Scholar 

  • Price, G.D., Day, D.A., Gresshoff, P.M. (1987) Rapid isolation of intact peribacteroid envelopes from soybean nodules and demonstration of selective permeability to metabolites. J. Plant Physiol.130, 157–164

    CAS  Google Scholar 

  • Reibach, P.H., Streeter, J.G. (1984) Evaluation of active versus passive uptake of metabolites byRhizobium japonicum bacteroids. J. Bacteriol.159, 47–52

    PubMed  CAS  Google Scholar 

  • Robertson, J.G., Farnden, K.J.F. (1984) Ultrastructure and metabolism of the developing legume root nodule. In: The biochemistry of plants, vol. 12, pp. 65–113, Davies, D.D., ed. Academic Press, New York

    Google Scholar 

  • Robertson, J.G., Lyttleton, P., Bullivant, S., Grayston, G.F. (1978) Membranes in lupin root nodules. I. The role of golgi bodies in the biogenesis of infection threads and peribacteroid membranes. J. Cell Sci30, 129–149

    PubMed  CAS  Google Scholar 

  • Robertson, J.G., Lyttleton, P., Tapper, B.A. (1984) The role of the peribacteroid membrane in legume root nodules. In: Advances in nitrogen fixation research, pp. 474–81, Veeger, C., Newton, W.E., eds. Nijhoff/Junk, Dordrecht, The Netherlands

    Google Scholar 

  • Ronson, C.W. (1988) Genetic regulation of C4-dicarboxylate transport in rhizobia. In: Nitrogen fixation: Hundred years after, pp. 541–551, Bothe, H., de Bruijn, F.J., Newton, W.E., eds. Fischer, Stuttgart, FRG

    Google Scholar 

  • Ronson, C.W., Lyttleton, P., Robertson, J.G. (1981) C4-dicarboxylate transport mutants ofRhizobium trifoli form ineffective nodules onTrifolium repens. Proc. Natl. Acad. Sci. USA78, 4284–4288

    PubMed  CAS  Google Scholar 

  • Schacterle, S.E., Pollack, R.L. (1978) Simplified method for quantitative assay of small amounts of protein in biological material. Anal. Biochem.51, 654–655

    Article  Google Scholar 

  • Stowers, M.D. (1985) Carbon metabolism inRhizobium species. Annu. Rev. Microbiol.39, 98–108

    Article  Google Scholar 

  • Streeter, J.G. (1981) Seasonal distribution of carbohydrates in nodules and stem exudate from field-grown soyabean plants. Ann. Bot.48, 441–450

    CAS  Google Scholar 

  • Streeter, J.G., Salminen, S.O. (1988) Carbon metabolism and the exchange of metabolites between symbionts in legume nodules. In: Physiological limitations and the genetic improvement of symbiotic nitrogen fixation, pp. 11–20, O'Gara, F.O., ed. Kluwer, Amsterdam

    Google Scholar 

  • Stumpf, D.K., Burris, R.H. (1979) A micromethod for the purification and quantification of organic acids of the tricarboxylic acid cycle in plant tissues. Anal. Biochem.95, 311–315

    Article  PubMed  CAS  Google Scholar 

  • Udvardi, M.K., Day, D.A. (1989) Electrogenic ATPase activity on the peribacteroid membrane of soybean (Glycine max L.) root nodules. Plant Physiol.90, 982–987

    PubMed  CAS  Google Scholar 

  • Udvardi, M.K., Price, G.D., Gresshoff, P.M., Day, D.A. (1988a) A dicarboxylate transporter on the peribacteroid membrane of soybean nodules. FEBS Lett.231, 36–40

    Article  CAS  Google Scholar 

  • Udvardi, M.K., Salom, C.S., Day, D.A. (1988b) Transport ofl-glutamate across the bacteroid but not the peribacteroid membrane from soybean root nodules. Mol Plant-Microbe Interact.1, 250–254

    Google Scholar 

  • Udvardi, M.K., Ou Yang L., Young, S., Day, D.A. (1990) Sugar and amminoacid transport across symbiotic membranes of soybean nodules. Mol. Plant-Microbe Interact., in press

  • Verma, D.P.S., Fortin, M.G., Stanley, J., Mauro, V.P., Purohit, S., Morrison, N. (1986) Nodulins and nodulin genes ofGlycine max. Plant Mol. Biol.7, 57–61

    Article  Google Scholar 

  • Werner, D., Dittrich, W., Thierfelder, H. (1982) Malonate and Krebs cycle intermediates utilization in the presence of other carbon sources byRhizobium japonicum and soybean bacteroids. Z. Naturforsch.37c, 921–926

    CAS  Google Scholar 

  • Zoglowek, C., Kromer, S., Heldt, H. (1988) Oxaloacetate and malate transport of plant mitochondria. Plant Physiol.87, 109–115

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Botany, Australian National University, GPO Box 4, 2601, Canberra, ACT, Australia

    Li-Jun Ou Yang, Michael K. Udvardi & David A. Day

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  1. Li-Jun Ou Yang
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  2. Michael K. Udvardi
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  3. David A. Day
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Ou Yang, LJ., Udvardi, M.K. & Day, D.A. Specificity and regulation of the dicarboxylate carrier on the peribacteroid membrane of soybean nodules. Planta 182, 437–444 (1990). https://doi.org/10.1007/BF02411397

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  • DOI: https://doi.org/10.1007/BF02411397

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