The Effect of Oxygen Concentration on Photosynthesis in Higher Plants

The influence of oxygen concentration in the range 0–21% on photosynthesis in intact leaves of a number of higher plants has been investigated. Photosynthetic Co₂ fixation of higher plants is markedly inhibited by oxygen in concentrations down to less than 2%. The inhibition increases with oxygen concentration and is about 30% in an atmosphere of 21% O₂ and 0.03% Co.₂. Undoubtedly, therefore, oxygen in normal air exerts a strong inhibitory effect on photosynthetic Co₂ fixation of land plants under natural conditions. The inhibitory effect of oxygen is rapidly produced and fully reversible. The degree of inhibition is independent of light intensity. The quantum yield for Co₂ fixation, i.e. the slope of the linear part of the curve for Co₂ uptake versus absorbed quanta, is inhibited to the same degree as the light saturated rate at all oxygen concentrations studied. Diverse species of higher plants, varying greatly in photosynthetic response to light intensity and Co₂ concentration, and with light saturated roles of Co₂ fixation differing by a factor of more than 10 times, show a remarkable similarity in their response to oxygen concentration. By contrast, when studied under the same conditions as the higher plants, the green algae Chlorella and Ulva did not show-any measurable inhibition of photosynthetic Co₂ fixation. Similarity, the increase in fluorescence intensity with increasing oxygen concentrations found in higher plants also was not seen in Chlorella. The present results, together with previous data on the photosynthetic response of algae to oxygen concentration, indicate that the photosynthetic apparatus of higher plants differs considerably from that of algae in its sensitivity to oxygen. The inhibitory effect of oxygen on photosynthetic Co₂ fixation in higher plants is somewhat higher at wavelengths which excite preferentially photosystem I. Also, the Emerson enhancement of Co₂ fixation measured when a far red beam of low intensity is imposed on a background of red light is greater under low oxygen concontrution than under air. Measurements of reversible light-induced absorbance changes reveal that the change at 591 nm, probably caused by pla.stocyanin, is affected by oxygen concentration only if photosystem II is excited. the reducing effect on plastocyanin, caused by excitation of this system, decreases with increasing oxygen concentration. From these results it is suggested that a possible site of the inhibition by oxygen is in the electron carrier chain between the two photosystems. Oxygen might act as an electron acceptor at this site, causing reducing power to react back with molecular oxygen. However, this hypothesis does not account for equal inhibitions of the quantum yield and the light saturated rate of photosynthetic CO₂ uptake. Through the photosynthetic process plants take up carbon dioxide and evolve oxygen. The present high concentration of molecular oxygen in the atmosphere is generally considered to have arisen from the activity of photo-synthetic organisms. The effect of oxygen concentration would seem, therefore, to he a problem of great interest, not only in the field of the biophysics and biochemistry of photosynthesis, but in ecology and other branches of biology as well. It was discovered by Warburg (1920) that high concentrations of oxygen inhibit the rate of photosynthetic oxygen evolution in the unicellular alga Chlorella. Since then, it has been confirmed by various authors that oxygen cconcentrations in the range 21–100 per cent have a marked inhibitory effect on photosynthesis, particularly at saturating light intensities. There is some evidence that under conditions when carbon dioxide concentration limits photosynthesis, the inhibition may become obvious even in 21 per cent oxygen. The inhibition has not been considered to operate at low light intensities. A review on the subject has been given by Turner and Brittain (1962). Various hypotheses have been put forward to explain the inhibitory effect of oxygen, commonly referred to as the Warhurg effect. Some authors favor the idea of enzyme inhibition; Turner et al. (1958) that one or more enzymes of the carbon reduction cycle are inactivated by oxygen: lirianlals (1962) that enzymes of the oxygen-evolving complex are inhihited. Other hypotheses concern back-reactions in which molecular oxygen is taken up, thus reversing the photosynthetic process. These reactions include photo-oxidation, photorespiration, and the Mehler reaction (Tamiya et al., 1957). At present, there is no generally accepted hypothesis explaining the effect. The often conflicting results on which these hypotheses were based have been obtained mostly on algae. The first observation of an inhibitory effect on photosynthesis in a higher plant was made hy McAlister and Myers (1940) in wheat leaves. They found that the photosyntlietic CO₂ uptake was markedly lower in air than in an atmosphere of about 0.5 per cent oxygen. At the CO₂ concentration used (0.03%) the inhibition was present both at high and moderate light intensities. No data were obtained at low light intensities. Although the study of the effect of oxygen concentration on photosynthesis in higher plants would seem to be of great interest, particularily since the natural environment of most land plants is an atmosphere with an oxygen content of 21 per cent, it has attracted very little attention. To the author's knowledge no thorough investigation on the subject has been published. The present investigalion is directed toward elucidatirng the photosynthetic response of higher plants to oxygen concentrations up to that of normal air. Data are presented showing that the photosynthetic CO₂ fixation in intact leaves of higher plants, regardless of light intensity, is strongly inhibited by oxygen in normal air, and that the pholosynthetic response to oxygen differs considerably from that of green algae. The present investigalion is directed toward elucidatirng the photosynthetic response of higher plants to oxygen concentrations up to that of normal air. Data are presented showing that the photosynthetic CO₂ fixation in intact leaves of higher plants, regardless of light intensity, is strongly inhibited by oxygen in normal air, and that the pholosynthetic response to oxygen differs considerably from that of green algae.