Inhibition of photosynthesis, acidification and stimulation of zeaxanthin formation in leaves by sulfur dioxide and reversal of these effects

Abstract

Leaves of Pelargonium zonale L. and Spinacia oleracea L. were fumigated with high concentrations of SO2 for very short periods of time with the aim of first producing acute symptoms of damage and then observing repair. The response of different photosynthetic parameters to SO2 was monitored during and after fumigation. The following results were obtained: (1) Inhibition of CO2 assimilation in the light was accompanied by increased reduction of the quinone acceptor, QA, of photosystem II and by increased oxidation of the electrondonor pigment P700 of photosystem I. Increased control of photosystem II activity in the SO2-inhibited state was also indicated by increased light scattering and by increased non-photochemical quenching of chlorophyll fluorescence. Both are indicators of chloroplast energization. Apparently, SO2 did not decrease but rather increased energization of the chloroplast thylakoid system by light. (2) Accumulation of dihydroxyacetone phosphate, fructose-1,6-phosphate and ribulose-1,5-phosphate and a decrease of 3-phosphoglycerate and hexosephosphate indicated that SO2 inhibited enzymes of the Calvin cycle. (3) Stimulated postillumination CO2 evolution suggested that when photosynthesis declined respiration increased to provide energy for repair reactions. (4) Increased leaf absorbance at 505 nm indicated increased stimulation of zeaxanthin formation in thylakoid membranes under the influence of SO2. A similar increase in 505-nm absorbance could be induced by high concentrations of CO2. In darkened leaves, SO2 did not produce changes in 505-nm absorbance. (5) While zeaxanthin formation was stimulated, changes in the fluorescence of the pH-indicating dye pyranine, which had been fed to the leaves, indicated acidification of the cytoplasm of leaf cells by SO2. Maximum acid production by SO2 required light. In contrast, cytoplasmic acidification of leaf cells by CO2 was similar in the light and in the dark. (6) Since zeaxanthin formation is known to depend on the acidification of the thylakoid lumen, SO2-dependent zeaxanthin formation indicated SO2-dependent acidification of the thylakoid lumen as the indirect result of cytoplasmic acidification by SO2. (7) Inhibition of photosynthesis and other effects of SO2 were fully reversible in the light. Detoxification of SO2 and reactivation of the photosynthetic apparatus were slow or absent in the dark. Light had a dual effect on the action of SO2. Transiently, it first increased the extent of inhibition of assimilation, but, finally, it reversed inhibition. Sulfur dioxide was inhibitory as a consequence of the chemical reactivity of its hydration products rather than as a result of cellular acidification by the produced acid. The initial acidification was followed by an appreciable alkalisation demonstrating the action of the pH-stat mechanism. (8) The data are discussed in relation to SO2 toxicity under field conditions when plants are chronically exposed to polluted air.