Light-Dependent Ion Translocation in Spinach Chloroplasts

The absorption of light by chloroplasts is the first step for several energy-requiring systems such as ATP synthesis and CO2 fixation. Recently, it has been found that light can alter the structure and volume of the chloroplast (7, 15, 17, 26). Therefore the question was raised whether light could affect ion movements in isolated chloroplasts under conditions where structural changes occur. This action of light on ion uptake by chloroplasts has received little attention, even though ion movements in algae and higher plants have been known for some time. Hoagland and Davis in 1923 were among the earliest in demonstrating a role of light in the movement of ions in plant cells by showing light-induced increases of chloride and bromide in Nitella cells (10). These observations were extended in 1934 by Jacques and Osterhout, who found that light increased the rate of K entry into Valonia macrophysa (16). Later, Arens reported Ca movements through Elodea leaves by a process dependent on photosynthesis (1), and Ingold found that chloride , K and phosphate were accumulated by such leaves in the light (14). Although subsequent investigations showed that lightdependent uptake of ions is a general process in plants (4, 19), still little is known about the mechanism of this process in chlorophyll-containing tissues. Certain features of the problem outlined above for chloroplasts are relevant to the properties of mitochondria. Mitochondria are known to regulate their structure and also to translocate ions by an energy-dependent mechanism. In 1961, Ca uptake by mitochondria was reported by Vasington and Murphy (32) and by DeLuca and Engstrom (6). Ca uptake in rat kidney mitochondria was dependent on respiration and required ATP, Mg, and phosphate (33). Ca binding was prevented by uncouplers of oxidative phosphorylation and electron-transport inhibitors. Brierley, M.urer, and Green found that ADP inhibited divalent cation uptake, possibly by competing with the ion for a high-energy intermediate (3). The close association of ion uptake with phosphorylation in mitochondria was shown by Rossi and Lehninger, who reported that for each pair of electrons traversing a phosphorvlating site in the respiratory chain, 1.0 molecules of phosphate and 1.67 of Ca were accumulated (29). During Ca and phosphate accumulation, other ions also undergo concentration changes; e.g., the intramitochondrial K content falls and Na rises, although only 2 to 3 % as much monovalent ion is moved as Ca (5). It now appears that ion uptake by plant mitochondria occurs under similar conditions as ion uptake by animal mitochondria (12, 22). By an approach initially based on mitochondrial investigations for the uptake of Ca and phosphate, it has now been discovered that the basic conditions of electron flow, Mg and ATP support the uptake of these ions by isolated spinach chloroplasts. [Preliminary reports of this research have recently appeared (24, 25)]. This ion translocation process is associated with the light-triggered Mg-activated hydrolysis of ATP in chloroplasts (11, 21, 28). The ability of spinach chloroplasts to take up other ions has been surveyed and it has been found that Na is also taken up by an energy-dependent process.