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PLANT PHYSIOLOGY , Vol 101, Issue 1 161-169, Copyright © 1993 by American Society of Plant Biologists
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PLANT-MICROBE INTERACTIONS |
Role of Oxygen in the Limitation and Inhibition of Nitrogenase Activity and Respiration Rate in Individual Soybean Nodules
M. M. Kuzma, S. Hunt and D. B. Layzell
Department of Biology, Queen's University, Kingston, Ontario, Canada, K7L 3N6
Although infected cell O2 concentration (Oi) is known to limit respiration
and nitrogenase activity in legume nodules, techniques have not been
available to measure both processes simultaneously in an individual legume
nodule. Consequently, details of the relationship between nitrogenase
activity and Oi are not fully appreciated. For the present study, a probe
was designed that allowed open circuit measurements of H2 evolution
(nitrogenase activity) and CO2 evolution (respiration rate) in a single
attached soybean nodule while simultaneously monitoring fractional
oxygenation of leghemoglobin (and thereby Oi) with a nodule oximeter.
Compared to measurements of whole nodulated roots, use of the probe led to
inhibition of nitrogenase activity in the single nodules. During oximetry
measurements, total nitrogenase activity (TNA; peak H2 evolution in Ar/O2)
in the single nodules was 16% of that in whole nodulated roots and 48% of
nodulated root activity when Oi was not being measured simultaneously. This
inhibition did not affect the nodules' ability to regulate Oi, because
exposure to Ar/O2 (80:20, v/v) caused nitrogenase activity and respiration
rate to decline, and this decline was linearly correlated with a concurrent
decrease in Oi. When the nodules were subsequently exposed to a linear
increase in external pO2 from 20 to 100% O2 at 2.7% O2/min, fractional
leghemoglobin oxygenation first increased gradually and then more rapidly,
reaching saturation at a pO2 between 76 and 100% O2. Plots of nitrogenase
activity and respiration rate against Oi showed that rates increased with
Oi up to a value of 57 nM, with half-maximal rates being attained at Oi
values between 10 and 14 nM O2. The maximum nitrogenase activity achieved
during the increase in pO2 (potential nitrogenase activity) was 30 to 57%
of that measured in intact nodulated roots, showing that O2 limitation of
nitrogenase activity could account for a significant proportion of the
inhibition of TNA associated with the use of the probe. However, some
factor(s) in addition to O2 must have limited the activity of single
nodules at both subsaturating and saturating Oi. At Oi values greater than
about 57 nM, nitrogenase activity and nodule respiration were inhibited,
but, because this inhibition has been shown previously to be readily
reversible when the Oi was lowered, it was not attributed to direct O2
inactivation of the nitrogenase protein. These results indicate that
maximum nitrogenase activity in legume nodules is supported by a narrow
range of Oi values. Possible biochemical mechanisms are discussed for both
O2 limitation of nitrogenase activity at low Oi and inhibition of
nitrogenase activity at high Oi.
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