Abstract
The rates of nodule O2, CO2, N2 and H2 exchange calculated in the previous modeling study (D.B. Layzell et al., 1987, Planta 173, 117–127) were combined with information on the diffusion characteristics of each gas, and the structural characteristics of soybean nodules, to produce a comprehensive mathematical model of nodule structure and function. The model assumed that an aqueous barrier to gas diffusion exists in the nodule cortex which may be regulated to maintain an O2 concentration of 10 nM in the centre of the infected cells of the central zone. The model was used to predict the concentration of N2, CO2 and H2 in the infected cells as the physical and physiological characteristics of the nodule were varied. The model predicted that (a) the diffusion barrier may be represented by plugs of water in the intercellular spaces of a layer of cells between the inner and outer cortex, the depth of which may be varied to vary the resistance of the barrier; (b) facilitated diffusion of O2 by oxyleghemoglobin is essential to the regulation of free O2 concentration in the infected cells; (c) the diffusion barrier is less effective in regulating CO2 flux than the fluxes of other gases with the result that the total gas pressure in the central zone is less than atmospheric pressure; (d) concentrations of N2 and HCO -3 in the infected cells are saturating with respect to nitrogenase activity and phosphoenolpyruvate carboxylase activity respectively and (e) under atmospheric conditions the concentration of H2 in the infected cells is similar to, or greater than the K i . (H2) for N2 fixation, which may account for values of nitrogenase electron allocation coefficient below 0.75.
Similar content being viewed by others
References
Appleby, C.A. (1969) Properties of leghemoglobin in vivo and its isolation as ferrous oxyleghemoglobin. Biochim. Biophys. Acta 188, 222–229
Atkins, C.A. (1974) Occurrence and some properties of carbonic anhydrases from legume root nodules. Phytochemistry 13, 93–98
Bergersen, F.J. (1982) Root nodules of legumes: Structure and functions. Research Studies Press, Toronto
Bergersen, F.J., Goodchild, D.J. (1973) Aeration pathways in soybean root nodules. Aust. J. Biol. Sci. 26, 729–740
Bergersen, F.J., Turner, G.L. (1980) Properties of terminal oxidase systems of bacteroids from root nodules of soybean and cowpea and of N2-fixing bacteria grown in continuous culture. J. Gen. Microbiol. 118, 235–252
Bethenod, O., Prioul, J.L., Deroche, M.E. (1985) Short-term inhibition of acetylene reduction activity by low CO2 concentrations around the nodulated roots of various legumes. Physiol. Vég. 22, 565–570
Bird, R.B., Stewart, W.E., Lightfoot, E.N. (1960) Transport phenomena. John Wiley & Sons, New York
Burris, R.H. (1985) H2 as a inhibitor of N2 fixation. Physiol. Vég. 23, 843–848
Dixon, R.O.D., Blunden, E.A.G., Searl, J.W. (1981) Intercellular space and hydrogen diffusion in pea and lupin root nodules. Plant Sci. Lett. 23, 109–116
Helder, R.J. (1985) Diffusion of inorganic carbon across an unstirred layer: a simplified quantitative approach. Plant Cell Env. 8, 399–408
Hunt, S., King, B.J., Cavin, D.T., Layzell, D.B. (1987) Steady and nonsteady state gas exchange characteristics of soybean nodules in relation to the oxygen diffusion barrier. Plant Physiol. 84, 164–172
Jensen, B.B. (1985) Isotope ratio mass spectrometry studies of HD formation by nitrogenase. In: Gas enzymology (Proc. of a Symp., Odense University, Denmark, May 1984), pp. 207–227, Degn, H., Cox, R.P., Toftlund, H., eds. D. Reidel Publishing Co., Boston
Layzell, D.B., Gaito, S.T., Hunt, S. (1987) Model of gas exchange and diffusion in legume nodules. I. Calculation of gas-exchange rates and the energy cost of N2 fixation. Planta 173, 117–127
Li, J., Burris, R.H. (1983) Influence of pN2 on HD formation by various nitrogenases. Biochemistry 22, 4472–4480
Minchin, F.R., Sheehy, J.E., Minguez, M.I., Witty, J.F. (1985) Characterisation of the resistance to oxygen diffusion in legume nodules. Ann. Bot. 55, 53–60
Peterson, J.B., Evans, H.J. (1979) Phosphoenolpyruvate carboxylase from soybean nodule cytosol. Evidence for isoenzymes and kinetics of the most active component. Biochim. Biophys. Acta 567, 445–452
Robson, R.L., Postgate, J.R. (1980) Oxygen and hydrogen in biological nitrogen fixation. Annu. Rev. Microbiol. 34, 183–207
Sheehy, J.E., Minchin, F.R., Witty, J.F. (1983) Biological control of the resistance to oxygen flux in nodules. Ann. Bot. 52, 565–572
Sheehy, J.E., Bergersen, F.J. (1986) A simulation study of the functional requirements and distribution of leghaemoglobin in relation to biological nitrogen fixation in legume root nodules. Ann. Bot. 58, 121–136
Sheehy, J.E., Minchin, F.R., Witty, J.F. (1985) Control of nitrogen fixation in a legume nodule: an analysis of the role of oxygen diffusion in relation to nodule structure. Ann. Bot. 55, 549–562
Sinclair, T.R., Goudriaan, J. (1981) Physical and morphological constraints on transport in nodules. Plant Physiol. 67, 143–145
Tjepkema, J.D., Cartica, R.J. (1982) Diffusion limitation of oxygen uptake and nitrogenase activity in root nodules of Parasponia rigida Merr. and Perry. Plant Physiol. 69, 728–733
Tjepkema, J.D., Yocum, C.S. (1973) Respiration and oxygen transport in soybean nodules. Planta 115, 59–72
Tjepkema, J.D., Yocum, C.S. (1974) Measurement of oxygen partial pressure within soybean nodules by oxygen microelectrode. Planta 119, 351–360
Umbreit, W.W., Burris, R.H., Stauffer, J.F. (1957) Manometric techniques. Burgess Publishing Co., Minneapolis, Minn., USA
White, D.C.S. (1974) Biological physics. Chapman and Hall, London
Witty, J.F., Minchin, F.R., Sheehy, J.E., Minguez, M.I. (1984) Acetylene-induced changes in the oxygen diffusion resistance and nitrogenase activity of legume root nodules. Ann. Bot. 53, 13–20
Witty, J.F., Minchin, F.R., Skot, L., Sheehy, J.E. (1986) Nitrogen fixation and oxygen in legume root nodules. Plant Molec. Cell Biol. 3, 277–314
Author information
Authors and Affiliations
Additional information
Abbreviations: See Appendix 1, and Appendix 1 in Layzell et al. (1987)
Rights and permissions
About this article
Cite this article
Hunt, S., Gaito, S.T. & Layzell, D.B. Model of gas exchange and diffusion in legume nodules. Planta 173, 128–141 (1988). https://doi.org/10.1007/BF00394497
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00394497