Summary
A simulation model is presented for the distribution and consumption of O2 in infected cells of soybean root nodule central tissue. It differs from earlier models in closer adherence to observed structure and embodies new morphometric data about the distribution of > 12,000 mitochondria per cell and about the geometry of the gas-filled intercellular spaces near which the mitochondria are located. The model cell is a rhombic dodecahedron and O2 enters only through interfaces (totalling 26% of the cell surface) with 24 gas-filled intercellular spaces. These spaces are located at the edges of each rhombic face of the cell, forming an interconnected network over the cell suface. Next, O2 is distributed through the cytoplasm by a leghaemoglobin-facilitated diffusive process, initially between the mitochondria and amyloplasts in the outer layers of the cell and then between > 6,000 symbiosomes (each containing 6 bacteroids) towards the central nucleus. The symbiosomes and mitochondria consume O2, but impede its diffusion; all O2 entering symbiosomes is considered to be consumed there. For the calculations, the cell is considered to consist of 24 structural units, each beneath one of the intercellular spaces, and each is divided into 126 layers, 0.2 μm thick, in and through which O2 is consumed and diffused. Rates of consumption of O2 and of N2 fixation in each diffusion layer were calculated from previously-established kinetics of respiration by mitochondria and bacteroids isolated from soybean nodules and from established relationships between bacteroid respiration and N2 fixation. The effects of varying the O2-supply concentration and the concentration and type of energy-yielding substrates were included in the simulations. When the model cell was supplied with 0.5 mM malate, mitochondria accounted for a minimum of 50% of the respiration of the model cell and this percentage increased with increased concentration of the O2 supply. Gradients of concentrations of free O2 dissolved in the cytoplasm were steepest near the cell surface and in this location respiration by mitochondria appeared to exert a marked protective effect for nitrogen fixation in layers deeper within the cell. Estimates of N2 fixation per nodule, calculated from the model cell, were similar to those calculated from field measurements.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- Lb:
-
leghaemoglobin
- LbO2 :
-
oxyleghaemoglobin
- [O2]:
-
concentration of free, dissolved O2
- e.m.:
-
electron micrograph
References
Appleby CA (1984) Leghaemoglobin andRhizobium respiration. Annu Rev Plant Physiol 35: 443–478
Bergersen FJ (1982) Root nodules of legumes: structure and functions. Research Studies Press/Wiley, Chichester
— (1978) Concluding remarks. Proc R Soc Lond [Biol] 317: 295–297
— (1993) Diffusion of oxyleghaemoglobin. Ann Bot 72: 577–582
—, Goodchild DJ (1973 a) Aeration pathways in soybean root nodules. Aust J Biol Sci 26: 729–740
— — (1973 b) Cellular location and concentration of leghaemoglobin in soybean root nodules. Aust J Biol Sci 26: 742–756
—, Turner GL (1992) Supply of O2 regulates O2 demand during utilization of reserves of poly-β-hydroxybutyrate in N2-fixing soybean bacteroids. Proc R Soc Lond [Biol] 249: 143–148
— — (1993) Effects of concentrations of substrates supplied to N2-flxing soybean bacteroids in flow chamber reactions. Proc R Soc Lond [Biol] 251: 95–102
— —, Gault RR, Chase DL, Brockwell J (1985) The natural abundance of15N in an irrigated soybean crop and its use for calculation of nitrogen fixation. Aust J Agric Res 36: 411–423
Crank J (1956) The mathematics of diffusion. Oxford, Clarendon Press
Denison RF (1992) Mathematical modeling of oxygen diffusion and respiration in legume root nodules. Plant Physiol 98: 901–907
—, Smith DL, Legros T, Layzell DB (1991) Noninvasive measurement of internal oxygen concentration of field-grown soybean nodules. Agron J 83: 166–169
Hunt S, Layzell DB (1993) Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu Rev Plant Physiol Plant Mol Biol 44: 483–511
—, Gaito ST, Layzell DB (1988) Model of gas exchange and diffusion in legume nodules II. Characterization of the diffusion barrier and estimation of the concentrations of CO2, H2 and N2 in infected cells. Planta 173: 128–141
King BJ, Hunt S, Weagle GE, Walsh KB, Pottier RH, Canvin DT, Layzell DB (1988) Regulation of O2 concentration in soybean nodules observed by in situ spectroscopic measurement of leghemoglobin oxygenation. Plant Physiol 87: 296–299
Kuzma MM, Hunt S, Layzell DB (1993) Role of oxygen in the limitation and inhibition of nitrogenase activity in individual soybean nodules. Plant Physiol 101: 161–169
Layzell DB, Gaito ST, Hunt S (1988) 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
—, Hunt S, Palmer GR (1990) Mechanism of nitrogenase inhibition in soybean nodules. Pulse-modulated spectroscopy indicates that nitrogenase activity is limited by O2. Plant Physiol 92: 1101–1107
Millar AH, Day DA, Bergersen FJ (1994) Microaerobic respiration of mitochondria from soybean roots and nodules. Plant Cell Environ (in press)
Sheehy JE, Bergersen FJ (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
— —, Minchin FR, Witty J (1987) A simulation study of gaseous diffusion resistance, nodule pressure gradients and biological nitrogen fixation in soybean nodules. Ann Bot 60: 345–351
Stewart I (1991) How to succeed in stacking. New Scientist 131: 23–26
Studer D, Hennecke H, Müller M (1992) High-pressure freezing of soybean nodules leads to improved preservation uf ultra-structure. Planta 188: 155–163
Thumfort PP, Atkins CA, Layzell DB (1994) A re-evaluation of the role of the infected cell in the control of O2 diffusion in legume nodules. Plant Physiol (in press)
Van Cauwenberghe OR, Newcomb W, Canny MJ, Layzell DB (1993) Dimensions and distribution of intercellular spaces in cryoplaned soybean nodules. Physiol Plant 89: 252–261
Wittenberg JB, Bergersen FJ, Appleby CA, Turner GL (1974) Facilitated diffusion. The role of leghemoglobin in nitrogen fixation by bacteroids isolated from soybean root nodules. J Biol Chem 249: 4057–4066
Author information
Authors and Affiliations
Additional information
Dedicated to the memory of Professor John G. Torrey
Rights and permissions
About this article
Cite this article
Bergersen, F.J. Distribution of O2 within infected cells of soybean root nodules: a new simulation. Protoplasma 183, 49–61 (1994). https://doi.org/10.1007/BF01276812
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01276812