Oxygen limitation of N<sub>2</sub> fixation in stem‐girdled and nitrate‐treated soybean

Vessey, J. Kevin; Walsh, Kerry B.; Layzell, David B.

doi:10.1111/j.1399-3054.1988.tb09201.x

Cited by 129 publications

(120 citation statements)

References 29 publications

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“…The gas permeability of legume nodules is of considerable current interest because nodule responses to drought, nitrate, and photosynthate supply all apparently involve changes in nodule 02 permeability (6,7,11,14,16,20,22). Similar permeability changes occur in response to acetylene exposure (12) or with increased or decreased external 02 concentration (23,27).…”

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confidence: 81%

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

Denison¹,

Layzell²

1991

Plant Physiol.

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Physiological regulation of nodule gas permeability has a central role in the response of legumes to such diverse factors as drought, defoliation, and soil nitrate. A new method for quantifying nodule respiration and 02 permeability, based on noninvasive spectrophotometry of leghemoglobin, was evaluated using intact, attached nodules of Lotus corniulatus. First permeability (6, 7, 11, 14, 16, 20, 22 (24) has not been seriously criticized, but the procedure is tedious, requiring chromatographic analysis of many gas samples for each permeability measurement.FOL,' determined by spectrophotometry in total darkness, has been used to estimate O0 in cut nodules (1), detached nodules (13), and nodules flattened during growth (9, 10). An improved, pulse-modulated method (11) allowed measurement of FOL in intact, attached nodules under ambient light. This method revealed that several treatments which inhibit nitrogen fixation also decrease 0,, under both laboratory (I 1) and field (6) conditions. It was concluded that lower Oi in inhibited nodules resulted from a decrease in nodule 02 permeability.The rate of increase of FOL, after switching the atmosphere around a nodule from nitrogen to oxygen, was greater for control nodules than for inhibited nodules. The rate ofchange of FOL represents a balance between 02 diffusion through the cortex and 02 consumption in the nodule interior. Therefore, it was suggested that a rapid increase in FOL could indicate relatively high 02 permeability (6,11

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confidence: 81%

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

Denison¹,

Layzell²

1991

Plant Physiol.

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“…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.…”

Section: Introductionmentioning

confidence: 99%

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confidence: 99%

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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“…In addition, carbohydrate is required either as an energy source or as an osmoticum to run ion pumps that act to increase or decrease resistance of O # diffusion into nodules (Vance & Heichel, 1991). Treatments that restrict carbohydrate supply to the nodules, such as NO $ − reduction (Vessey et al, 1988a,b ;Walsh, 1990), light deprivation (Minchin et al, 1985) ; nodule excision (Hunt et al, 1987), defoliation (Hartwig et al, 1987), and stem girdling (Vessey et al, 1988b), increase O # diffusion resistance into nodules and subsequently lower nitrogenase activity. On the other hand, treatments that increase carbohydrate supply to nodules, such as increased irradiance (Bethlenfalvay & Phillips, 1978 ;Houwaard, 1980), can alleviate NO $ − inhibition.…”

Section: Research Interactive Effects Of Co # and Soil N On N # -Fixamentioning

confidence: 99%

Nitrogen inhibition of nodulation and N₂ fixation of a tropical N₂‐fixing tree (Gliricidia sepium) grown in elevated atmospheric CO₂

2000

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Interactive effects of elevated atmospheric CO# and soil N availability on N # fixation and biomass production were examined using Gliricidia sepium, a tropical leguminous tree species. Our objective was to determine if elevated CO # alters the inhibitory effects of soil N on N # fixation, and whether the response of Gliricidia to elevated CO # was a function of N source originating from either substrate N fertilizer or N # fixation. We hypothesized that CO # enrichment would ameliorate the inhibitory effects of N fertilization on seedling nodulation and N # fixation through increased C partitioning to nodules. Seedlings were grown from seed for 100 d in growth chambers at either 350 or 700 µmol mol −" CO # . Seedlings were inoculated with Rhizobium spp. and grown either with 0, 1 or 10 mM N fertilizer. The δ"&N isotope-dilution technique was used to determine N source partitioning between N # fixation and inorganic N fertilizer uptake. The addition of 10 mM N fertilizer significantly reduced nodule number and mass, specific nitrogenase activity, the specific rate of N # fixation, and the proportion of plant N derived from N # fixation. Elevated CO # , however, strongly ameliorated the inhibitory effects of N fertilization, indicating that increased C availability for nodule activity may partially offset the inhibition of N # fixation caused by substrate N, as nodule sugar concentrations were stimulated with CO # enrichment. This study clearly shows that elevated CO # enhanced plant productivity and net N content of Gliricidia tree seedlings by stimulating N # fixation. In addition, seedling biomass production was greatly enhanced by elevated CO # , regardless of whether plant N was derived from the substrate or from the atmosphere. We conclude from this study that CO # enrichment mitigates the inhibitory effects of substrate N on nodule initiation and development and specific N # fixation, either through increased C allocation to nodule production and activity, or through increased N demand by the plant for biomass production. This experiment with Gliricidia provides evidence for a positive feedback between increased atmospheric CO # concentrations, C allocation to symbiotic N # -fixing bacteria, and plant C and N accumulation that may occur when N # -fixing plants are grown under conditions where substrate N may typically inhibit N # fixation.

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Oxygen limitation of N₂ fixation in stem‐girdled and nitrate‐treated soybean

Cited by 129 publications

References 29 publications

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

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

Mathematical Modeling of Oxygen Diffusion and Respiration in Legume Root Nodules

Nitrogen inhibition of nodulation and N₂ fixation of a tropical N₂‐fixing tree (Gliricidia sepium) grown in elevated atmospheric CO₂

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Oxygen limitation of N2 fixation in stem‐girdled and nitrate‐treated soybean

Cited by 129 publications

References 29 publications

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

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

Mathematical Modeling of Oxygen Diffusion and Respiration in Legume Root Nodules

Nitrogen inhibition of nodulation and N2 fixation of a tropical N2‐fixing tree (Gliricidia sepium) grown in elevated atmospheric CO2

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Oxygen limitation of N₂ fixation in stem‐girdled and nitrate‐treated soybean

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

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

Nitrogen inhibition of nodulation and N₂ fixation of a tropical N₂‐fixing tree (Gliricidia sepium) grown in elevated atmospheric CO₂