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Antimycin a Stimulation of Rate-Limiting Steps of Photosynthesis in Isolated Spinach Chloroplastst

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Antimycin a Stimulation of Rate-Limiting Steps of Photosynthesis in Isolated Spinach Chloroplastst Plant Physiol. (1972) 49, 411-416 Antimycin A Stimulation of Rate-limiting Steps of Photosynthesis in Isolated Spinach Chloroplastst Received for publication September 13, 1971 BERNICE SCHACTER2 I AND JAMES A. BASSHAM Laboratory of Chemical Biodynamics, Lawrence Berkeley Laboratory, University of California, Berkeley, California 94720 ABSTRACT The effects of antimycin A addition on the levels of labeled metabolites formed during photosynthesis by isolated, whole Changes in levels of metabolites in isolated spinach (Spinacia spinach chloroplasts are examined in this report. Also, the ef- oleracea) chloroplasts seen upon addition of antimycin A sug- fects of antimycin A on the transport of gest that the activities of enzymes mediating several regulated metabolites from the reactions are the of added chloroplasts were followed to determine if any changes in affected. Apparently, presence transport could be related to the stimulatory effects of anti- antimycin A does not increase the level of C02 in the chloro- mycin A. plasts, nor does it stimulate C02 fixation by increasing the level of the carboxylation substrate, ribulose-1, 5-diphosphate. Rather, it appears that antimycin A increases C02 fixation rate MATERIALS AND METHODS by indirectly stimulating the enzyme, ribulose-1,5-diphosphate Chloroplasts were isolated from spinach (Spinacia oleracea) carboxylase (E.C. 4.1.1.39), which mediates the carboxylation leaves, and the rate of '4CO2 fixation was determined as pre- of ribulose-1, 5-diphosphate to give 3-phosphoglycerate. An- viously described, with the exception that unless noted, iso- other rate-limiting enzyme of the reductive pentose phosphate ascorbate was omitted from all solutions (18). Analysis of the cycle, hexose diphosphatase (E.C. 3.1.3.11), seems also to be "C and 'P-labeled products of photosynthesis by two-dimen- stimulated. The synthesis of polysaccharides (mostly starch) sional chromatography and radioautography was carried out seems also to be stimulated. These results are interpreted as as described earlier (23). Estimation of the distribution of indicating that antimycin A addition enhances the general acti- metabolites between the chloroplasts and the surrounding me- vation of those enzymes which already are activated during dium was also carried out as previously described (8). The "4C photosynthesis but are inactive in the dark. The ratio of aden- radioactivity found at the origin was taken as a measure of osine triphosphate-adenosine diphosphate under conditions of the synthesis of "C-labeled starch and other polysaccharides. photosynthesis was only moderately decreased in the presence With whole cells, following photosynthesis with "CO2, acid of antimycin A, perhaps accounting in part for an observed in- hydrolysis of this insoluble material at the origin gives glu- crease in accumulation of 3-phosphoglycerate as compared with cose, amino acid, and nucleic acid components (20, 21). Spin- dihydroxyacetone phosphate. No significant effect on movement ach chloroplasts, isolated and allowed to photosynthesize with of metabolites from the chloroplast to the medium was seen. "CO2 as described previously (12), produce essentially only polysaccharides as insoluble end products, since such chloro- plasts form only negligible amounts of amino acids. Chlorophyll was determined by the method of Arnon (1). Antimycin A was obtained from Sigma Chemical Co. and dissolved in absolute ethanol. The total concentration of etha- nol was kept at 1 % or less, and, unless indicated, all controls Antimycin A has been reported to stimulate the rate of contained 1% ethanol. photosynthesis of isolated spinach chloroplasts, as measured by the rate of bicarbonate uptake (11, 12, 15, 26). Identifica- tion of the site of action of this stimulation and determination RESULTS of the mechanism of stimulation could aid in the general un- In the earlier reports of the antimycin A stimulation of derstanding of the control of the photosynthetic metabolism. CO2 fixation with chloroplasts, the control rates were generally The action of antimycin A as an inhibitor and uncoupler of low-10 to 35 ,wmoles CO2 fixed/mg chlhr (11. 12, 26). An photoelectron transport and phosphorylation in chloroplast early observation in the present study was that chloroplasts fragments has been previously reported (2, 3, 14, 16, 17, 28, with CO2 fixation rates of 130 ,umoles/mg chl-hr were stimu- 29). Several observations have led to proposals that antimycin lated by 0.5 [kM antimycin A to C02 fixation rates of 180 A stimulates the rate of CO2 fixation in intact chloroplasts by ,umoles/mg chl-hr. While the control rates and the magnitude stimulating the transport or activation of CO2 or bicarbonate of the antimycin A stimulation varied with the spinach used, for the carboxylation step (12, 26). the presence of antimycin A (0.5-5.0 [LM) in the incubation mixture from the start of the experiment dependably gave 1 This work was supported in part by the United States Atomic large stimulations over the control rate. A typical result is Energy Commission. given in Figure 1. In the case where antimycin A was added 2 Charles F. Kettering Postdoctoral Fellow, 1970-1971. at the beginning of the experiment the CO2 fixation rate (118 'Present address: Department of Pharmacology, University of ,umoles/mg chl 'hr) during the first 5 min was stimulated 79% Miami, Miami, Fla. 33136 over the control rate. When antimycin A was added after 5- 411 412 SCHACTER AND BASSHAM Plant Physiol. Vol. 49, 1972 creased bicarbonate (Figs. 9 and 10) are completely different 24 / / from the changes due to antimycin A addition (Figs. 4 and 5). 0 The increase in SDP with increased bicarbonate concentration a was typical of the changes in all intermediates examined 0 -C (starch, PGA, DHAP, FDP, F6P, etc.) except for RuDP, - which clearly, and as predicted, dropped upon increasing the 16 Antimycin A * E bicarbonate concentration. IN ,~/ As previously reported (12, 26), antimycin A stimulated the x rate of CO2 fixation at both limiting and saturating bicarbon- ate concentrations. The metabolic consequences of added anti- mycin A were also similar at both bicarbonate concentrations, 0 8 as shown by the levels of SDP and RuDP in Figures 11 and 12. 2) Since it had been demonstrated that regulatory factors 0 E (PPi, Mge, and a factor associated with spinach alkaline FDPase) can have marked effects on the transport or release of metabolites from the chloroplasts into the surrounding me- 0 4 8 12 dium (6), it was of interest to determine if antimycin A might MIN. be exerting its stimulatory effects by changing the pattern of FIG. 1. Rates of CO2 fixation by isolated spinach chloroplasts transport of metabolites from the chloroplasts. An examina- with added antimycin A. (broken line): Control with 10 gl tion of the distribution between chloroplasts and the surround- ethanol added (rate = 66,moles C02/mg chl*hr during ing medium of the Calvin cycle intermediates labeled during min); (solid line): control with 10 Al of ethanol added at min photosynthesis showed no significant changes in movement of = (rate 53 C02/mg chl-hr during 7- to 12-min interval); ,umoles metabolites into the medium in response to antimycin A. A (broken line): antimycin A added at the beginning of experiment Because antimycin A has frequently been demonstrated to (rate 118,umoles chl-hr during first 5 min); A (solid CO2/mg uncouple both cyclic and noncyclic photophosphorylation in line): antimycin added at 5 min (rate 106 /moles CO2/mg chl-hr during 7- to 12-min interval). chloroplast fragments (14), we examined the effect of anti- mycin A on the levels of ATP in intact chloroplasts before and during photosynthesis by following the incorporation of min photosynthesis, the subsequent rate (106 ,umoles/mg 'P, into ATP both in the presence and absence of bicarbon- chl-hr) was 100% higher than the control rate (53,umoles/mg ate. The data presented in Figure 13 were obtained by incu- chl - hr). bating chloroplasts in the presence and absence of 0.5 The experiment which gave the data shown in Figure 1 was /M antimycin A, first during an air, light preincubation, and then performed with no preincubation and an argon gas phase. Ad- after the addition of bicarbonate. There was no significant dition of antimycin A to chloroplasts after the usual light, air, change in the accumulation of 'P1 into ATP in the absence preincubation and 2 to 5 min photosynthesis in the presence of bicarbonate. Upon addition of bicarbonate, a slightly greater of bicarbonate sometimes gave little or no stimulation. Exclu- decrease in the labeled pool of ATP was seen in the chloro- sion of air seems to be required to obtain the stimulation re- plasts incubated with antimycin A. Since the rate of CO2 fixa- producibly. Moreover, the inclusion of 10 mm isoascorbate, tion was increased in this instance by antimycin A from 74 to usually a standard component of the incubation mixture for 141,umoles fixed/mg chl hr, the actual rate of synthesis of chloroplasts (18), also prevented the stimulatory response to ATP must be correspondingly greater in the chloroplasts in- antimycin A, even if the antibiotic were initially present. Un- cubated with antimycin A than in the control chloroplasts. less noted, therefore, isoascorbate was routinely omitted from Thus the decreased level of ATP might be due only to the the reaction mixture, and an argon atmosphere was provided. increased demand for ATP compared to its rate of synthesis. The effects of the addition during photosynthesis of anti- This may also account for the drop in labeled ATP observed mycin A on the incorporation of"4C into several intermediates upon the addition of antimycin A to photosynthesizing chloro- of the Calvin cycle are shown in Figures 2 to 8. The increase plasts (Fig. 14). in 3-PGA and RuDP, and the drop in SDP and in FDP, oc- It was also found that the stimulation of CO2 fixation by curred consistently upon the addition of antimycin A, but the antimycin A is somewhat sensitive to the concentration of increase in starch and decrease in F6P occurred only if the added Mg2_ (Fig.
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