Measurement of Legume Nodule Respiration and O<sub>2</sub> Permeability by Noninvasive Spectrophotometry of Leghemoglobin

Denison, R. Ford; Layzell, David B.

doi:10.1104/pp.96.1.137

Cited by 49 publications

(65 citation statements)

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“…All infected cells were assumed to be identical, so the total 02 uptake was the uptake per infected cell times the number of infected cells per nodule. (6). As a quantitative test of the unsteady-state 02 method, these calculated values were compared with those assumed by the model.…”

Section: Computation Methods and Parametersmentioning

confidence: 99%

“…The permeability that is often observed (6,19) or if there were other unresolvable discrepancies between predicted and actual nodule behavior.…”

mentioning

confidence: 99%

“…Modeling was also used to assess the role of Lb' in 02 transport and to evaluate possible sources oferror in a recently developed noninvasive assay for nodule respiration and 02 permeability (6). Some additional calculations addressed the possible contribution of cytoplasmic streaming to oxygen transport in nodules.…”

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confidence: 99%

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Mathematical Modeling of Oxygen Diffusion and Respiration in Legume Root Nodules

Denison¹

1992

Plant Physiol.

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The 02 permeability of legume root nodules is under physiological control; decreases in permeability are triggered by various forms of stress. Two linked mathematical models were used to explore several hypotheses concerning the physical nature of the variable diffusion barrier in nodules. Respiration and diffusion of dissolved 02 and oxygenated leghemoglobin were simulated for the nodule cortex and the nodule interior. Measured nodule permeabilities were shown to be inconsistent with the hypothesis that large numbers of air-filled pores penetrate the diffusion barrier. Changes in the affinity of leghemoglobin for 02 or in the rate of cytoplasmic streaming in diffusion barrier cells did not result in the large changes in 02 permeability reported for real nodules. The presence or absence, but not the thickness, of aqueous plugs in radial pores through the cortex was found to have a large effect on permeability. Flooding of intercellular spaces, either between layers of cells in the cortex or in the nodule interior, also caused large changes in simulated permeability. The unsteady-state 02 method for determining nodule permeability was tested using data generated by the model. The accuracy of the method was confirmed, provided that certain assumptions (full oxygenation of leghemoglobin under pure 02 and uniform conditions in the nodule interior) are met.A diffusion barrier in legume root nodules restricts 02 flux into the nodule and thereby protects nitrogenase from inactivation by 02 (21,22). The responses of nodules to such seemingly unrelated factors as drought, nitrate, and defoliation all apparently involve changes in the gas permeability of this barrier (8,10,14,17,23,24 Variable gas permeability of nodules might result from changes in (a) the number or size of gas-filled radial pores through the barrier, (b) the thickness of water plugs in radial pores, (c) the extent of flooding between layers of cells, or (d) flooding of airspaces in the central zone.Under the "open pore" and "variable plug thickness" hypotheses, changes in nodule gas permeability result from changes in radial intercellular pores through a layer of closely packed cells in the nodule cortex. The open pore hypothesis postulates a low-resistance pathway through radial air-filled pores. Because the diffusion coefficient of 02 in air is 1O4 times that in water, diffusion through even a small number of open pores could dominate total diffusion (which also includes diffusion through cells) across the barrier. The low solubility of 02 in water or cytoplasm further decreases the diffusion rate in cells relative to air. It has been suggested that changes in either the radius (19,25) or the number (1 1) of open pores could control permeability. Under the variable plug thickness hypothesis (1 1), each pore contains a plug of water, and permeability depends on the thickness of the plug.The "flooded cortex" and "flooded interior" hypotheses have not previously been formulated explicitly. The

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Section: Computation Methods and Parametersmentioning

confidence: 99%

“…The permeability that is often observed (6,19) or if there were other unresolvable discrepancies between predicted and actual nodule behavior.…”

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confidence: 99%

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Mathematical Modeling of Oxygen Diffusion and Respiration in Legume Root Nodules

Denison¹

1992

Plant Physiol.

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“…Over a similar range of average free [O 2 ] in infected cells [11-63 nM in Fig. 3a; calculated from average FOL as in oximetry (Denison & Layzell 1991)], the gas space interface [O 2 ] was predicted to range from 40 to 3600 nM (approximately 0·003-0·3% in the gas phase). Average [O 2 ], calculated as an arithmetic average, ranged from 11 to 117 nM (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…1 The average fractional oxygenation of leghaemoglobin (FOL avg ) is a commonly used indicator of tissue oxygenation in nodules (Bergersen 1962;Appleby 1984;King et al 1988;Monroe, Owens & LaRue 1989;Layzell, Hunt & Palmer 1990;Denison & Layzell 1991;Kuzma et al 1993 Thumfort et al 1994).…”

Section: Calculation Of Predictionsmentioning

confidence: 99%

Diffusion and reaction of oxygen in the central tissue of ureide‐producing legume nodules

Thumfort

Layzell

Atkins

1999

Plant Cell & Environment

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It is not surprising then that the uricase reaction is believed to be severely limited by O 2 supply in vivo (Rainbird & Atkins 1981;Atkins 1991). If the pathway of purine synthesis was not closely regulated, accumulation of relatively insoluble uric acid could possibly limit the flux of fixed N from the nodule. However, cowpea nodules do not show measurable accumulation of uric acid (Atkins et al. 1988) and, even under conditions of reduced external pO 2 , ureide synthesis is maintained at a high rate (Atkins, Dakora & Storer 1990). Thus, either the affinity of uricase for O 2 is much higher in vivo than measured for the purified enzyme in vitro or the [O 2 ] in uninfected cells is considerably higher than that in adjacent infected cells. High intracellular [O 2 ] (Oi) in uninfected cells requires high pO 2 in the intercellular gas spaces, yet such concentrations are incompatible with a view of nodule functioning that does not allow for a resistance to O 2 entry into the infected cell .Most previous mathematical models for the diffusion and reaction of O 2 in nodules assumed [O 2 ] within the cytosol of the infected cell would be close to being equilibrated with pO 2 in the intercellular gas spaces of the tissue (Bergersen 1982;Sheehy et al. 1987;Gaito, Hunt & Layzell 1989;Bergersen 1994). Thus pO 2 in the intercellular gas spaces needed to satisfy uricase would be expected to raise Oi in the infected cells above the range in which nitrogenase activity is maintained. However, more recent simulations of diffusion into infected cells (Thumfort, Atkins & Layzell 1994, Thumfort, Layzell & Atkins 1999 predicted that saturation of leghaemoglobin (Lb) in the cyosol close to the cell : gas space interface would limit facilitated diffusion and provide an intrinsic mechanism for a variable diffusive resistance to O 2 entry. Bergersen (1996) also predicted significant gradients of [O 2 ] in the cytosol of infected cells, but attributed this to disequilibrium between O 2 and Lb due to loading of deoxygenated Lb near the cell surface. This region of the cell also shows a concentration of organelles (mitochondria and plastids) so that the volume of cytosol and amount of Lb is significantly reduced compared to the rest of the infected cell (Millar, Day & Bergersen et al. 1995). One consequence to resistance at this point in the diffusive pathway is that pO 2 in the gas spaces surrounding both infected and uninfected cells could be as high as 1-2% (12-25 mM;Thumfort et al. 1994Thumfort et al. , 1999 but would still maintain average Oi levels in infected cells as low as 10-60 nM. Such high pO 2 in the gas spaces could satisfy the low affinity of uricase for O 2 .All earlier mathematical models of nodules considered a central zone tissue comprising only infected cells and intercellular gas spaces. The present study models the diffusion and metabolism of O 2 more realistically. A geometrically detailed computer simulation was developed to incorporate the three-dimensional shape and packing of both cell types, at the f...

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Electron Microscopic Investigation of Water Occlusions in Intercellular Spaces in the Inner Cortex of Lucerne Nodules

Weisbach

Walther

Hartwig

et al. 1999

Journal of Structural Biology

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Measurement of Legume Nodule Respiration and O₂ Permeability by Noninvasive Spectrophotometry of Leghemoglobin

Cited by 49 publications

References 24 publications

Mathematical Modeling of Oxygen Diffusion and Respiration in Legume Root Nodules

Mathematical Modeling of Oxygen Diffusion and Respiration in Legume Root Nodules

Diffusion and reaction of oxygen in the central tissue of ureide‐producing legume nodules

Electron Microscopic Investigation of Water Occlusions in Intercellular Spaces in the Inner Cortex of Lucerne Nodules

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Measurement of Legume Nodule Respiration and O2 Permeability by Noninvasive Spectrophotometry of Leghemoglobin

Cited by 49 publications

References 24 publications

Mathematical Modeling of Oxygen Diffusion and Respiration in Legume Root Nodules

Mathematical Modeling of Oxygen Diffusion and Respiration in Legume Root Nodules

Diffusion and reaction of oxygen in the central tissue of ureide‐producing legume nodules

Electron Microscopic Investigation of Water Occlusions in Intercellular Spaces in the Inner Cortex of Lucerne Nodules

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Measurement of Legume Nodule Respiration and O₂ Permeability by Noninvasive Spectrophotometry of Leghemoglobin