Oxygen and light accelerate recovery from SO2-induced inhibition of leaf photosynthesis and from cytoplasmic acidification

Abstract

Leaves of several plant species were illuminated either in air or in a gas atmosphere with reduced oxygen content, and photosynthesis and transpiration were recorded after brief exposure to high concentrations of SO2. Inhibition of photosynthesis by SO2 was similar in air and at reduced oxygen concentrations or, in some experiments, even larger under low oxygen. Recovery from inhibition was always faster in high than in low oxygen. In leaves of Pelargonium zonale, stomata remained open or closed only slowly after fumigation, whereas in spinach and potato leaves stomata closed rapidly under the influence of high SO2. After cessation of fumigation, stomata always reopened. pH-indicating fluorescent dyes were employed to monitor SO2-dependent pH changes in the apoplast and the cytosol of leaf tissue. In the cytosol, acidification was weaker in the dark than in the light. In the light, it was stronger in 21 % oxygen than in 1 % oxygen. Cytosolic acidification could not fully be attributed to the hydration and oxidation of SO2 but was also caused by a transient breakdown of transmembrane proton gradients that resulted in the influx of acid from acidic leaf compartments into the cytosol. This was concluded from opposite pH changes in the cytosol and the apoplast under the influence of SO2. Even chloroplasts were transiently acidified by SO2 as shown by the kinetics of 505 nm absorption, which reflect the pH-sensitive interconversion of violaxanthin to zeaxanthin. Differences in the kinetics of SO2-dependent inhibition of photosynthesis and of cytosolic acidification in high and low oxygen suggest combined nucleophilic attack of sulfite, and of radicals generated in the light, on sensitive cellular constituents. However, the reversibility of photosynthesis inhibition and of acidification, particularly in the presence of air levels of oxygen, demonstrates fast repair. The observations suggest that detrimental effects on plants caused by long-term exposure to ambient concentrations of SO2, which are several hundredfold lower than used in the present investigation, can neither be explained by radical damage nor by immediate effects of cellular acidification. Both radical detoxification and pH regulation are highly effective in healthy plants.