Inhibition of Photosystem II Precedes Thylakoid Membrane Lipid Peroxidation in Bisulfite-Treated Leaves of Phaseolus vulgaris

Abstract

Exposure of leaves to S02 or bisulfite is known to induce peroxidation of thylakoid lipids and to inhibit photosynthetic electron transport. In the present study, we have examined the temporal relationship between bisulfite-induced thylakoid lipid peroxidation and inhibition of electron transport in an attempt to clarify the primary mechanism of S02 phytotoxicity. Primary leaves of bean (Phaseolus vulgaris L. cv Kinghom) were floated on a solution of NaHSO3, and the effects of this treatment on photosynthetic electron transport were determined in vivo by measurements of chlorophyll a fluorescence induction and in vitro by biochemical measurements of the light reactions using isolated thylakoids. Lipid peroxidation in treated leaves was followed by monitoring ethane emission from leaf segments and by measuring changes in fatty acid composition and lipid fluidity in isolated thylakoids. A 1 hour treatment with bisulfite inhibited photosystem 11 (PSII) activity by 70% without modifying Photosystem 1, and this inhibitory effect was not light-dependent. By contrast, lipid peroxidation was not detectable until after the inhibition of PSII and was strongly light dependent. This temporal separation of events together with the differential effect of light suggests that bisulfite-induced inhibition of PSII is not a secondary effect of lipid peroxidation and that bisulfite acts directly on one or more components of PSII.Sulfur dioxide is a wide-spread air pollutant that produces a variety of toxic effects in plants (26,30). A primary site of action appears to be the photosynthetic apparatus as indicated by the inhibition of CO2 fixation during the early stages of SO2 toxicity (15,30). This is supported by the observed inhibition of a number of partial reactions of photosynthesis after exposure to SO2 or its related anionic forms, sulfite and bisulfite (1,10,12,28,29). Photosynthetic electron transport is particularly sensitive, apparently as a result of inhibition of PSII (12,28,29).The mechanism of action of sulfur dioxide has not been clearly established, although it has been suggested that induction of thylakoid lipid peroxidation is involved (25). Indeed, there is considerable evidence that sulfur dioxide damages plant membranes by facilitating free radical-mediated lipid peroxidation (8,24). The oxidation of sulfur dioxide in solution (as sulfite) is known to occur by a chain reaction that can be initiated by a variety of free radical-generating agents including illuminated chloroplasts (3, 26). During propagation of the reaction, the free radicals, OH. (hydroxyl), S03-. (sulfite), and 02-(superoxide), are thought to be generated (14,26), although recent spin-trapping evidence suggests that S03-is more important than 02-in the propagation of chloroplast-initiated oxidation of the sulfite ion (1 1). The free radicals generated are thought to be responsible for the observed peroxidation ofthylakoid lipids exposed to sulfite (17).Several studies, considered together, implicate thylakoid membrane lipid peroxidatio...

Ozone, Sulfur Dioxide, and Ultraviolet B Have Similar Effects on mRNA Accumulation of Antioxidant Genes in Nicotiana plumbaginifolia L

“…In each case, PSII seems to be the major target site (Schreiber et al, 1978;Covello et al, 1989;Renger et al, 1989;Strid et al, 1990). As a consequence, plant metabolic processes involved in fatty acid degradation may be activated for energy supply.…”

Factors altering the membrane fluidity of spinach thylakoid as determined by fluorescence polarization

“…In contrast, the control membrane sample displayed a low g level and a high fluidity with a P value around 0.3, which is similar to previously reported P value ranging from 0.25 to 0.36 in thylakoid membranes of pea with highly unsaturated lipids (Barber et al 1980). The early work by Covello et al (1989) showed that treatment with 20 mM NaHSO 3 led to an increase in P value of thylakoid membranes in primary bean leaves from 0.185 to 0.320, which was associated with a decrease in PSII-driven electron transport and an enhanced ethane production. Li et al (2007) reported that a large quantity of reactive oxygen species was induced by bisulfite stress.…”

“…Chloroplast lipids are known to contain a higher proportion of unsaturated fatty acid (Hiller and Raison 1980), thylakoid lipids contain an abundant of alpha-linolenic acid (18:3) and slightly lower levels of palmitic acid (16:0) and LA (18:2) (Covello et al 1989). Linolenic acid (18:3) at high concentration has been reported to induce a significant decrease of P value in pea thylakoid membrane (Barber et al 1980).…”

Effect of Decreasing Oxygen Concentration on Plant Metabolism in Response to Different Environmental Stresses.

“…The prodon concentration of the cytoplasm is one of the most important factors regulating cellulase activity When cells are exposed to SO 2 an appreciable acidification of the cytoplasm occur because this gas reacts with water to form sulfurous acid which may then be converted into Sulphuric acid (112,113,114). These results, in loss of photosynthetic function caused by inhibition of the activity of SH-containing light-activated enzymes of the inhibition of the activity of SH-containing light-activated enzymes of the chloroplast (115,116,117).…”