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Effect of oxygen pressure on synthesis and export of nitrogenous solutes by nodules of cowpea

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Abstract

Nodules of cowpea plants (Vigna unguiculata (L.) Walp. cv. Vita 3 :Bradyrhizobium CB756) cultured for periods of 23 d with their root systems maintained in atmospheres containing a range of partial pressures of O2 (pO2; 1–80%, v/v, in N2) formed and exported ureides (allantoin and allantoic acid) as the major products of fixation at all pO2 tested. In sub-ambient pO2 (1 and 2.5%) nodules contained specific activities of uricase (urate: O2 oxidoreductase; EC 1.7.3.3) and allantoinase (allantoin hydrolyase; EC 3.5.2.5) as much as sevenfold higher than in those from air. On a cell basis, uninfected cells in nodules from 1% O2 contained around five times the level of uricase. Except for NAD: glutamate synthase (EC 1.4.1.14), which was reduced in sub-ambient O2, the activities of other enzymes of ureide synthesis were relatively unaffected by pO2. Short-term effects of pO2 on assimilation of fixed nitrogen were measured in nodules of air-grown plants exposed to subambient pO2 (1, 2.5 or 5%, v/v in N2) and15N2. Despite a fall in total15N2 fixation, ureide synthesis and export was maintained at a high level except in 1% O2 where formation was halved. The data indicate that in addition to the structural and diffusional adaptations of cowpea nodules which allow the balance between O2 supply and demand to be maintained over a wide range of pO2, nodules also show evidence of biochemical adaptations which maintain and enhance normal pathways for the assimilation of fixed nitrogen.

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Abbreviations

GOGAT:

glutamate synthase (glutamine oxo-glutarate amidotransferase)

GS:

glutamine synthetase

pO2 :

partial pressure of oxygen in the gas phase

References

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

    Article  CAS  Google Scholar 

  • Atkins, C.A. Rainbird, R.M., Pate, J.S. (1980) Evidence for a purine pathway of ureide synthesis in N2-fixing nodules of cowpea (Vigna unguiculata (L.) Walp.). Z. Pflanzenphysiol.97, 249–260

    CAS  Google Scholar 

  • Atkins, C.A., Shelp, B.J., Storer, P.J. (1985) Purification and properties of inosine monophosphate oxidoreductase from nitrogen-fixing nodules of cowpea (Vigna unguiculata L. Walp.). Arch. Biochem. Biophys.236, 807–814

    Article  CAS  PubMed  Google Scholar 

  • Atkins, C.A., Storer, P.J., Pate, J.S. (1988) Pathways of nitrogen assimilation in cowpea nodules studied using15N2 and allopurinol. Plant Physiol.86, 204–207

    CAS  Google Scholar 

  • Atkins, C.A., Storer, P.J., Shelp, B.J. (1989) Purification and properties of purine nucleosidase from nitrogen-fixing nodules of cowpea (Vigna unguiculata L. Walp.). J. Plant Physiol.134, 447–452

    CAS  Google Scholar 

  • Bergersen, F.J., Goodchild, D.J. (1973) Aeration pathways in soybean root nodules. Aust. J. Biol. Sci.26, 729–740

    Google Scholar 

  • Chen, F.L., Cullimore, J.V. (1988) Two isoenzymes of NADH-dependent glutamate synthase in root nodules ofPhaseolus vulgaris L. Plant Physiol.88, 1411–1417

    CAS  Google Scholar 

  • Cullimore, J.V., Lea, P.J., Miflin, B.J. (1982) Multiple forms of glutamine synthetase in the plant fraction ofPhaseolus root nodules. Isr. J. Bot.31, 151–162

    Google Scholar 

  • Dakora, F.D., Atkins, C.A. (1989) Diffusion of oxygen in relation to structure and function in legume root nodules. Aust. J. Plant Physiol.16, 131–140

    CAS  Google Scholar 

  • Dakora, F.D., Atkins, C.A. (1990a) Effect of pO2 on growth and nodule functioning of symbiotic cowpea (Vigna unguiculata L. Walp.). Plant Physiol.93, 948–955

    CAS  Google Scholar 

  • Dakora, F.D., Atkins, C.A. (1990b) Effect of pO2 during growth on the gaseous diffusional properties of nodules of cowpea (Vigna unguiculata L. Walp.). Plant Physiol.93, 956–961

    CAS  Google Scholar 

  • Dakora, F.D., Atkins, C.A. (1990c) Morphological and structural adaptation of nodules of cowpea to functioning under sub- and supra-ambient pO2. Planta182, 572–582

    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 

  • Govers, F., Moerman, M., Hooymans, J., Van Kammen, A., Bisseling, T. (1986) Microaerobiosis is not involved in the induction of pea nodulin-gene expression. Planta169, 513–517

    Article  CAS  Google Scholar 

  • Hanks, J.F., Tolbert, N.E., Schubert, K.R. (1981) Localisation of enzymes of ureide biosynthesis in peroxisomes and microbodies of nodules. Plant Physiol.68, 65–69

    CAS  Google Scholar 

  • Hanks, J.F., Schubert, K.R., Tolbert, N.E. (1983) Isolation and characterisation of infected and uninfected cells from soybean nodules. Plant Physiol.71, 869–873

    CAS  Google Scholar 

  • Larsen, K., Jochimsen, B.U. (1986) Expression of nodule-specific uricase in soybean callus tissue is regulated by O2. EMBO J.5, 15–19

    CAS  PubMed  Google Scholar 

  • Larsen, K., Jochimsen, B.U. (1987) Appearance of purine-catabolizing enzymes in fix+ and fix- root nodules on soybean and effect of O2 on the expression of the enzymes in callus tissue. Plant Physiol.85, 452–456

    CAS  Google Scholar 

  • Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J. (1951) Protein measurement with Folin phenol reagent. J. Biol. Chem.193, 265–276

    CAS  PubMed  Google Scholar 

  • Martinek, K., Berezin, I.V., Khmelnitski, Y.L., Klyachko, N.L., Levashov, A.V. (1987) Micellar enzymology: potentialities in applied areas (biotechnology). Coll. Czech. Chem. Commun.52, 2589–2602

    CAS  Google Scholar 

  • Nguyen, T., Zelechwska, M., Foster, V., Bergmann, H., Verma, D.P.S. (1985) Primary structure of the soybean nodulin-35 gene encoding uricase II localised in the peroxisomes of uninfected cells of nodules. Proc. Natl. Acad. Sci. USA85, 5020–5024

    Google Scholar 

  • Ohyama, T., Kumazawa, K. (1980) Nitrogen assimilation in soybean nodules. III. Effects of rhizosphere pO2 on the assimilation of15N2 in nodules attached to intact plants. Soil Sci. Plant Nutr.26, 321–324

    CAS  Google Scholar 

  • Pate, J.S., Peoples, M.B., Storer, P.J., Atkins, C.A. (1985) Extrafloral nectaries of cowpea (Vigna unguiculata L., Walp.). II. Nectar composition, origin of nectar solutes and nectary functioning. Planta166, 28–38

    Article  CAS  Google Scholar 

  • Rainbird, R.M., Atkins, C.A. (1981) Purification and some properties of urate oxidase from nitrogen-fixing nodules of cowpea (Vigna unguiculata L. Walp.). Biochem. Biophys. Acta659, 132–140

    CAS  PubMed  Google Scholar 

  • Rawsthorne, S., LaRue, T.A. (1986) Metabolism under microaerobic conditions of mitochondria from cowpea nodules. Plant Physiol.81, 1097–1102

    CAS  Google Scholar 

  • Shelp, B.J., Atkins, C.A., Storer, P.J., Canvin, D.T. (1983) Cellular and subcellular organisation of pathways of ammonia assimilation and ureide synthesis in nodules of cowpea (Vigna unguiculata L. Walp.) Arch. Biochem. Biophys.224, 429–441

    Article  CAS  PubMed  Google Scholar 

  • Theimer, R.R., Beevers, H. (1971) Uricase and allantoinase in glyoxysomes. Plant Physiol.45, 246–251

    Google Scholar 

  • Trijbels, F., Vogels, G.D. (1966) Degradation of allantoin byPseudomonas acidovorans. Biochim. Biophys. Acta113, 292–301

    CAS  PubMed  Google Scholar 

  • Van den Bosch, K.A., Newcomb, E.H. (1986) Immunogold localisation of nodule-specific uricase in developing soybean root nodules. Planta167, 425–436

    Article  Google Scholar 

  • Webb, M.A., Newcomb, E.H. (1987) Cellular compartmentation of ureide biogenesis in root nodules of cowpea (Vigna unguiculata L. Walp.). Planta172, 162–175

    Article  CAS  Google Scholar 

  • Witty, J.F., Minchin, F.R., Skot, L., Sheeny, J.E. (1986) Nitrogen fixation and oxygen in legume root nodules. Oxford Surveys Plant Mol. Cell Biol.3, 275–314

    CAS  Google Scholar 

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This work was supported by a grant from the Australian Research Council (to C.A.A.) and an Australian Development Assistance Bureau postgraduate fellowship (to F.D.D.).

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Atkins, C.A., Dakora, F.D. & Storer, P.J. Effect of oxygen pressure on synthesis and export of nitrogenous solutes by nodules of cowpea. Planta 182, 565–571 (1990). https://doi.org/10.1007/BF02341033

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