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Effects of Adenine Nucleotides on Hydrogen-Ion Transport in Chloroplasts

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Effects of Adenine Nucleotides on Hydrogen-Ion Transport in Chloroplasts Proc. Nat. Acad. Sci. USA Vol. 68, No. 10, pp. 2522-2526, October 1971 Effects of Adenine Nucleotides on Hydrogen-Ion Transport in Chloroplasts* (spinach/coupling factor 1/photophosphorylation/electron transport/ membrane permeability) RICHARD E. McCARTY, JONATHAN S. FUHRMAN, AND YOKO TSUCHIYA Section of Biochemistry and Molecular Biology, Cornell University, Ithaca, New York 14850 Communicated by Leon A. Heppel, July 23, 1971 ABSTRACT 1-10 tM ATP stimulated H+ uptake and tional change may reduce the permeability of the membranes slowed the release of H+ in the dark in chloroplasts illu- to H+. These observations help to explain theresults of Karlish minated at pH values at which photophosphorylation can occur, but not at pH 6.5. This ATP stimulation of H + up- and Avron (7) and why ADP and ATP inhibit electron trans- take was abolished by an antiserum to the chloroplast port (9). coupling factor and was reduced by the energy transfer inhibitors phlorizin and Dio-9. ATP synthesis after illu- MATERIALS AND METHODS mination was also enhanced by ATP. Electron flow from water to methyl viologen was inhibited by the same low Chloroplasts were prepared (10), from spinach purchased lo- concentrations of ATP. cally. Subehloroplast particles were prepared by exposure of ADP also increased the extent of H+ uptake in chloro- chloroplasts to sonic oscillation (11). Chlorophyll was esti- plasts, even in the presence of arsenate and MgCI2. In mated by the method of Arnon (12). the presence of hexokinase and glucose, as well as arsenate H+ uptake was measured at 20'C (13), except that 0.4-1.5 and Mig ++, ADP inhibited H + uptake. The failure of previ- ous investigators to observe a direct inhibition of H+ up- mM Tricine. NaOH or (,7Nr-(morpholino) ethane sulfonate take by phosphorylation was probably caused by a mask- (MES) NaOH were present. The buffer capacity of the sus- ing of the inhibition by the stimulation of H + uptake by pension was determined as described by Polya and Jagendorf ATP. Furthermore, the stimulation of H+ uptake by ATP (14). ATP formation after illumination was assayed by a modi- provides an explanation for its inhibition of electron flow. fication of the method of Hind and Jagendorf (15). The dark Although there is little doubt that the energy stored in gradi- reaction mixture contained 100 mM Tricine NaOH (pH 8), ents of H+ concentration across chloroplast membranes may 3 mM ADP, 2 mMlI potassium phosphate buffer, and carrier- be used to drive the synthesis of ATP (1), the relationship free 32p1 equivalent to 2-5 X 106 cpm, in a final volume of 0.5 between light-dependent H+ uptake (2) and photophosphor- ml. The light reaction mixture contained in a volume of 0.5 ml, ylation is not clear. In general, H+ uptake in chloroplasts has either 10 mM MES NaOH (pH 6) or 10 mM Tricine NaOH properties remarkably similar to those predicted by the chemi- (pH 8), 0.05 mM N-methylphenazonium methosulfate (PMS) osmotic theory of Mitchell (3). H+ uptake is sensitive to or pyocyanin, 50 mM NaCl, 5 mM MgCl2, and chloroplasts uncouplers of photophosphorylation (2) and generates rather (equivalent to 0.1 mg of chlorophyll). After illumination for large transmembrane gradients in H+ concentration (4, 5). 30 see with about 1 X 106 ergs/cm2 per see of white light at If the H+ gradient were the driving force for phosphoryla- 40C, the light reaction mixture was injected into the dark tion, or if ATP synthesis and H+ uptake are driven by a reaction mixture, which was maintained at 0-40C. The reac- common intermediate, phosphorylation should decrease the tion was terminated after 15 see by the addition of 0.05 ml of extent of H+ uptake. The accumulation of either NH4+ (6) 40% trichloroacetic acid and, after centrifugation, aliquots or of ethylamine (5) in spinach chloroplasts, which is a reflec- of the supernatant fluid were assayed for esterified 32P, (16). tion of H+ uptake, is inhibited by phosphorylation. In con- The Hill reaction, with methylviologen as the electron ac- trast, H+ uptake in lettuce chloroplasts was found by Karlish ceptor, was assayed polarographically with a Clark-type oxy- and Avron (7) to be stimulated by the simultaneous presence gen electrode. The reaction mixture was identical to that used of ADP, Pi, and Mg++. However, Dilley and Shavit (8) in the H+-uptake experiments, except that 0.1 mM methyl- presented evidence that this stimulation might be caused by a viologen was substituted for the pyocyanin or PMS, and that stimulation of electron flow by ADP or MgCl2 under the condi- 1 mM NaN3 was present. Photophosphorylation was deter- tions of low-salt concentration used by Karlish and Avroin (7). mined as described (10). In this paper, we report that ATP and ADP stimulate H+ Hexokinase was desalted before use on a 1 X 15 cm column uptake, as well as ATP synthesis in spinach chloroplasts after of Sephadex G-50 (medium), equilibrated with 25 mM sodium illumination. We suggest that coupling-factor 1 (CF1) alters acetate buffer (pH 5.4) that contained 50 m.M glucose. Hexo- its conformation on binding ADP or ATP. This conforma- kinase activity was determined enzymatically at pH 7.6 and 20'C. 1 unit is that amount of enzyme that catalyzes the formation of 1 ,umol of glucose 6-phosphate per min. Abbreviations: Tricine for Tris-(hydroxymethyl) methyl glycine; MES for N-(morpholino) ethane sulfonate; CF1 for chloroplast Nucleotides and PMIS were purchased from Sigma. The coupling factor 1; PMS for N-methyl phenazonium metho- ATP analogs (a,#- and 3,-y-methylene ATP) were from Miles sulfate; CCP for carbonylcyanide-m-chlorophenylhydrazone; Laboratories. Pyocyanin was prepared from PMS according to and STN for a solution containing 0.4 M sucrose-0.02 M Tri- Jagendorf and Margulies (17). Dio-9 was supplied by Dr. R. cine-NaOH (pH 8)-0.01 M NaCl. J. Guillory. Hexokinase was from Boehringer-Mlannheim. 2522 Downloaded by guest on September 29, 2021 Proc. Nat. Acad. Sci. USA 68 (1971) ATP Effects on H + Uptake 2523 0.20 Q. a_ 0 0 0 E =0 0.16 CPm 0*C E 0s 0) I- 0) -D 0) C -,0 0.12 a ,0-5_D Q. I. I 0.08), 10 20 30 40 50 60 70 pH ATP-pM FIG. 1. Effect of pH on the stimulation of H + uptake by FIG. 2. Effect of ATP concentration on H + uptake. The ATP. The reaction mixture (3 ml) contained 50 mM NaCl, reaction mixture was the same as that described in Fig. 1, except 5 mM MgCl,. 0.05 mM pyocyanin, chloroplasts equivalent to that the Tricine concentration was 1.5 mM. The pH was 7.60. 0.3 mg of chlorophyll, and the following buffers: MES-NaOH 1.66-2.33 mM for pH 6-7 and Tricine-NaOH 1.33 mM for pH frequently biphasic (Fig. 3). During the first 8-10 sec in the 7.5-8.5. dark, the decay in the presence of ATP was fast, although not as fast as that observed in the absence of ATP. The remainder Rabbit serum containing antibodies to CF1 was kindly pro- of the decay was usually considerably slower. In the presence vided by Dr. R. J. Berzborn. of methylviologen, the dark decay in the presence and absence of ATP was monophasic, and pronounced inhibitions of the RESULTS rate of the dark decay were observed. Although it is clear that ATP reduced the rate of the pH decay in the dark, it is not Stimulation of H + uptake by ATP readily possible to correlate this rate reduction by ATP to the The extent of light-dependent H+ uptake supported by cyclic increased extent of H+ uptake because of the complex kinetics. electron flow was stimulated by ATP when the assays were performed at pH values where phosphorylation takes place (Fig. 1). Maximal stimulation was observed at pH 8; no effect 8 MV PYO of ATP was detected at pH 6.5, the optimal pH for H+ up- (0.075) take. Generally, ATP stimulated the extent of H+ uptake at pH 7.6 by 40-60%. In some experiments, this stimulation was 4. as great as 250%, or as low as 20%. As little as 1 uM ATP stimulated H+ uptake (Fig. 2). Half- maximal stimulation was given by 3 AM ATP; saturation was achieved at 10 MM. H+ uptake in subchloroplast particles pre- CY 2 EATPo ttP pared by exposure of chloroplasts to sonic oscillation (11) was also enhanced by ATP. 0. Although ATP stimulated H+ uptake in the absence of added Mg++, 1 mM EDTA abolished this effect of ATP. If, however, 1 mM MgCl2 was present, EDTA did not prevent l.lmTrion)mh) the ATP stimulation of H+ uptake. Thus, Mg++-ATP, rather than ATP itself, is probably the stimulator. Neither arsenate nor Pi, at concentrations up to 1 mM af- 0.5 -ATP fected the ATP stimulation of H+ uptake. Since the endoge- -ATP nous Pi concentrations in our chloroplast preparations are low (about 0.07 ;imol/mg of chlorophyll), it is unlikely that the small amount of Pi contributed by the chloroplasts to the reac- tion mixture (about 7 AM) was enough to satisfy a Pi require- 02~ 6 20 ~30 0 lb 20 30 ment for the ATP stimulation. Avron et al. (9) reported that Time-sec the ATP inhibition of electron flow was unaffected by Pi. rise in the dark FIG. 3. Effect of ATP on the decay of the pH rise after At pH 7.6, the decay of the light-induced pH illumination.
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