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Chloroplast Membranes (Photosynthesis/Chloroplast Structure/Chloroplast Function/Reaction Center/Membrane Differentiation) JAN M

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Chloroplast Membranes (Photosynthesis/Chloroplast Structure/Chloroplast Function/Reaction Center/Membrane Differentiation) JAN M Proc. Natl Acad. Sci. USA Vol. 80, pp. 745-749, February 1983 Biophysics Localization of different photosystems in separate regions of chloroplast membranes (photosynthesis/chloroplast structure/chloroplast function/reaction center/membrane differentiation) JAN M. ANDERSON AND ANASTASIOS MELIS Division of Molecular Plant Biology, 313 Hilgard Hall, University of California, Berkeley, California 94720 Communicated by Daniel I. Amnon, November 4, 1982 ABSTRACT The stoichiometric amounts and the photoactiv- led to the hypothesis ofPSII heterogeneity in higherplant chlo- ity kinetics ofphotosystem I (PSI) and of the a and fl components roplasts (9). Analysis of the biphasic kinetics of PSII showed a of photosystem I (PSiH. and PSll^) were compared in spinach fast and nonexponential a component (PSIIa) and a slower ex- chloroplast membrane (thylakoid) fractions derived from ap- ponential (3 component (PSII,). The two types of PSII reaction pressed and nonappressed regions. Stroma-exposed thylakoid center complexes differ both in the effective light-harvesting fractions from the nonappressed regions were isolated by differ- Chl antenna size (10) and in the apparent midpoint redox po- ential centrifugation following a mechanical press treatment ofthe tential oftheir primary electron acceptor Q (11, 12). Mg2e ions chloroplasts. Thylakoid vesicles derived mainly from the ap- affect the organization of PSII. in the membrane but not that pressed membranes of grana were isolated by the aqueous poly- of PSII1l (13). Melis and Homann (13) proposed that PSII is mer two-phase partition method. Stroma-exposed thylakoids were located in grana partitions and PSII3 is located in stroma ex- foundtohaveachlorophylla/chlorophyllbratioof6.0andaPSII/ posed thylakoids. Further studies (14, 15) supported this con- PSI reaction center ratio of0.3. Kinetic analysis ofsystem II pho- cept, because the amounts of PSIIa and PSII, differed in mu- toactivity revealed the absence ofPSII, from stroma-exposed thy- tant tobacco compared with wild type, with PSII, increasing as lakoids. The photoactivity ofsystem Iin stroma-exposed thylakoids the amount of appressed relative to nonappressed membrane showed a single kinetic component identical to that ofunfraction- areaincreased. Hitherto, however, this hypothesis has not been ated chloroplasts, suggesting that PSI does not receive excitation the amounts ofthe two types ofPSII re- energy from the PSII-chlorophyll ab light-harvesting complex. tested by determining thylakoids are significantly enriched in both action center complexes in subthylakoid fractions. Thus, stroma-exposed In this paper, we report on the stoichiometric ratios and ki- PSI and PSp. Inside-out vesicles from the appressed membranes and PSI reaction ofgrana-partition regions had a chlorophyll a/chlorophyll b ratio netic properties of the photoactivity of PSII of2.0 and a PSI/PSI reaction center ratio of 10.0. The photoac- centers in thylakoid membrane fractions derived from grana tivity of system II showed the membranes of the grana-partition partitions and alsofrom stroma thylakoids. The results show that regions to be significantly enriched in PSI~,. We conclude that PSIIH is found exclusively in the grana-partition regions. In con- PSIIa is exclusively located in the membranes of the grana par- trast, stroma thylakoids are enriched in both PSI and PSII,,. titions while PSII, and PSI are located in stroma-exposed thyla- koids. The low PSI reaction center (P700) content of vesicles de- MATERIALS AND METHODS ofthe PSI rived from grana partitions and the kinetic homogeneity Chloroplasts were isolated from leaves of spinach (Spinacia complex suggest total exclusion ofP700 as a functional component the Yeda grana-partition region. oleracea L.). The chloroplast isolation procedure, in the membrane of the press treatment, and the aqueous polymer two-phase partition mem- methods were similar to those described in ref. 5. Stoichio- The structural differentiation ofhigher plant chloroplast PSII and PSI reaction centers were branes into grana stacks and stroma-exposed thylakoids is par- metric measurements of with stroma-exposed thy- taken with a sensitive optical difference spectrophotometer (8). alleled by a functional differentiation, The geometry ofthe apparatus and the experimental conditions lakoids having mainly photosystem (PS) I and grana stacks being have been reported (16, 17). For enriched in PSII (1). The introduction ofaqueous polymer two- for the kinetic measurements inside- determination of the primary photoactivity kinetics of the PSI phase partition by Albertsson (2) allowed the isolation of chloroplasts were first treated with cy- out vesicles derived mainly from grana partitions-i.e., the ap- reaction center (P700), even more anide for 60 min to inhibit plastocyanin (18). The Chl concen- pressed membranes of the grana stacks-that were Chl b ratios were determined according enriched in PSII (3, 4). Andersson and Anderson (5) demon- trations and the a/Chl strated a marked lateral heterogeneity in the distribution ofthe to ref. 19. chlorophyll (Chl)-protein complexes along the thylakoid mem- brane of spinach chloroplasts. Thylakoid membrane vesicles RESULTS derived from the granapartitions showed an enrichment in PSII To avoid the use of harsh detergents, which might disturb the Chl-protein complex and its associated Chl ab-protein of the in vivo organization ofthe supramolecular complexes ofthe thy- light-harvesting complex (LHC) and a substantial depletion in lakoids, the chloroplasts were fractionated mechanically by the PSI Chl-protein complex. These results led to the hypothesis Yeda press treatment. The Yeda press fractionation ofthe spin- that PSI is excluded from the grana-partition regions (5, 6). In ach thylakoids was followed by separation of the grana stacks contrast, stroma-exposed thylakoids were enriched in PSI but (Y-40) from the stroma-exposed thylakoids (Y-100) by differ- they always contained a small complement of PSII (5-8). ential centrifugation (5). We then used the aqueous polymer Recognition of the biphasic nature of PSII photoactivity has two-phase partition (2) to separate the right-side-out vesicles Abbreviations: Chl, chlorophyll; PS, photosystem; LHC, light-har- The publication costs ofthis article were defrayed in part by page charge primary electron ac- payment. This article must therefore be hereby marked "advertise- vesting complex; P700, reaction center of PSI; Q, ment" in accordance with 18 U. S. C. §1734 solely to indicate this fact. ceptor of PSII. 745 Downloaded by guest on September 26, 2021 746 Biophysics: Anderson and Melis Proc. Natl. Acad. Sci. USA 80 (1983) (fraction T-2), with both PSI and PSII characteristics, from the Time, s inside-out vesicles (fraction B-3), which are highly enriched in 0 0.2 0.4 PSII and are derived mainly from the granapartitions (3-5). The -. amounts of PSI and PSII reaction centers were measured di- rectly from the light-induced oxidation of the P700 (PSI) and A from the light-induced reduction of Q, the primary electron acceptor of PSII. I I The Chl a/Chl b ratios and the Q and P700 contents of un- 0ID~~~-d fractionated thylakoids and various subchloroplast fractions de- rived from appressed and nonappressed membrane regions are compared in Table 1. In mature unfractionated chloroplasts, the Chl a/Chl b ratio was about 2.8 and the ratios Chl/P700 = 580 and Chl/Q = 297 were comparable with those reported (20) for a variety ofhigher plant chloroplasts. Thus, spinach thylakoids appeared to have almost twice as much PSII reaction center as PSI reaction center (Q/P700 = 1.95). The stroma-exposed thylakoid membranes (fraction Y-100) FIG. 1. Kinetic traces: time course of P700 photooxidation. (A) derived from the Yeda press treatment (5) had a Chl a/Chl b Unfractionated chloroplasts at 238 ,uM Chl (a+b) in the presence of ratio ofabout 6 and were significantly enriched in PSI. The Q/ 200 puM methylviologen. Chl a/Chl b = 2.79; result presented is the P700 ratio was 0.3 in agreement mean of 16 individual measurements; AA700 = lo-3 (B) Isolated with a previous study (8). In stromathylakoidsat 23 ,IMChl (a+b) inthe presence of 200 p.M meth- contrast, the inside-out thylakoid vesicles, fraction B-3 derived ylviologen. Chl a/Chl b = 6.0; result presented is the mean of 32 in- mainly from the chloroplast partition regions, had a low Chl a/ dividual measurements; AA700 = 5 x 10'. Before fractionation, the Chl b ratio (about 2.1) and were markedly enriched in PSII (Q/ isolated chloroplasts were treated with cyanide to inhibit plastocyanin P700 = 9.6). As expected from theirknown photochemical char- (18). acteristics (4), the right-side-out vesicles (fraction T-2) from the grana, were slightly depleted in Q relative to chloroplasts (Table functionally homogeneous, in contrast to the observed heter- 1). ogeneity of PSII in higher plant thylakoids (9-15). Hence, a Comparison of the amount of P700 in stroma-exposed thy- careful comparison of the kinetics of the PSI photoactivity was lakoids (Y-100) with that in the grana partitions (B-3) shows a undertaken for unfractionated chloroplasts and the stroma thy- 10-fold depletion ofP700 in fraction B-3 relative to Y-100 (Table lakoid fraction (Y-100). 1). This is similar to the depletion of the PSI complex assayed The photooxidation kinetics of P700 induced by weak con- previously by NaDodSO4/polyacrylamide gel electrophoresis tinuous illumination is shown in Fig. 1. In this approach, the (5). Since fraction B-3 is known to be contaminated with right- rate of P700 photooxidation is limited by the rate of light ab- side-out vesicles (4), the depletion of P700 from the membrane sorption by PSI. The rate of light absorption by each PSI unit ofthe partition region must be greater in vivo than that detected depends directly on the antenna size of the light-harvesting in this study. These results support the concept of the lateral pigments associated with PSI. In principle then, one can obtain separation ofthe two photosystems in the thylakoid membrane an accurate estimate of the antenna size of the light-harvesting ofhigher plant chloroplasts (see Discussion).
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