Regulation of Soybean Nitrogen Fixation in Response to Rhizosphere Oxygen

Abstract

ABSTRACINodule nitrogen fixation rates are regulated by a mechanism which is responsive to the rhizosphere oxygen concentration. In some legumes, this oxygen-sensitive mechanism appears to involve changes in the gas permeability of a diffusion barrier in the nodule cortex. In soybean evidence for such a mechanism has not been found. The purpose of this research was to make quantitative measurements of soybean nodule ps permeability to test the hypothesis that soybean nodule gas permeability is under physiological control and responsive to the rhizosphere oxygen concentration. Intact hydroponically grown soybean plants were exposed to altered rhizosphere oxygen concentrations, and the nodule gas permeability, acetylene reduction and nodule respiration rates were repeatedly assayed. After a change in the external oxygen concentration, nitrogenase activity and nodule respiration rates displayed a short-term transient response after which the values returned to rates similar to those observed under ambient oxygen conditions. In contrast to steady-state nitrogenase activity and nodule respiration, nodule gas permeability was dramatically affected by the change in oxygen concentration. Decreasing the external oxygen concentration to 0.1 cubic millimeter per cubic millimeter resulted in a mean increase in nodule gas permeability of 63%. Increasing the rhizosphere oxygen concentration resulted in decreased nodule ps permeability. These data are consistent with the hypothesis that soybean nodules are capable of regulating nitrogen fixation and nodule respiration rates in response to changes in the rhizosphere oxygen concentration and indicate that the regulatory mechanism involves physiological control of the nodule gas permeability.When the rhizosphere oxygen concentration around intact soybean plants is altered over a range of 0.06 to 0.4 mm3 mm-3, nitrogenase activity and nodule respiration are independent of the external oxygen concentration after an initial transient period (3,4,17 where J is the oxygen flux (mm3 mm-2 s-') crossing the diffusion barrier, Oex is the rhizosphere oxygen concentration (mm3 mm 3),°in is the oxygen concentration (mm3 mm-3) in the intercellular air spaces around the bacteroid infected cells inside of the diffusion barrer, and P, is the gas permeability of the diffusion barrier (mm s-' ). Since the oxygen concentrations used in Equation 1 are in the gas phase, Ps contains the oxygen solubility and is defined aswhere D is the oxygen diffusion coefficient in cytoplasm (mm2 sI'), Sis the oxygen solubility in cytoplasm, and L is the thickness ofthe diffusion barrier (mm). As Oi,, is many orders ofmagnitude below ex, Equation 1 can be simplified to J = Ps Oex.In the experiments described by Weisz and Sinclair (17), Oex was increased from ambient (0.2 mm3 mm-3) to as high as 0.4 mm3 mm 3 oxygen without any long-term effects on nodule activity. Equation 3 predicts that for a change in Oe, a proportional change in J will also occur unless the permeability (Ps) changes as well. Thus, to maintain a l...

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

“…A decrease in permeability following an increase in 0e has previously been reported (9,23 (Fig. 3A).…”

“…Similar permeability changes occur in response to acetylene exposure (12) or with increased or decreased external 02 concentration (23,27). Studies with microelectrodes (19,27) and theoretical considerations (18) suggest that nodule permeability is limited mainly by one or more layers of tightly packed cells in the nodule cortex.…”

Mathematical Modeling of Oxygen Diffusion and Respiration in Legume Root Nodules

“…Indeed, estimates of nodule permeability made by the method of Sheehy et al (19) are based on nodule respiration rate. It should also be noted that changes in nodule permeability to acetylene (9) and ethylene (25), neither of which is carried by Lb, parallel changes in nodule permeability to 02 (Table III). For the flooded interior case, Vmax was estimated correctly, but the other two parameters were not.…”

“…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 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). Similar permeability changes allow nodules to acclimate to increased or decreased external 02 concentration (25,29).…”