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Adjustments of Photosystem Stoichiometry in Chloroplasts Proc. Natl. Acad. Sci. USA Vol. 87, pp. 7502-7506, October 1990 Botany Adjustments of photosystem stoichiometry in chloroplasts improve the quantum efficiency of photosynthesis (thylakoids/chloroplast acclimation/reaction center/quantum yield/light quality) WAH SOON CHOW*t, ANASTASIOS MELISt, AND JAN M. ANDERSON* *Commonwealth Scientific and Industrial Organisation, Division of Plant Industry, G.P.O. Box 1600, Canberra, Australian Capital Territory 2601, Australia; and *Department of Plant Biology, University of California, Berkeley, CA 94720 Communicated by Daniel L. Arnon, July 3, 1990 ABSTRACT The efficiency of photosynthetic electron apparatus, given the contrasting light environments in differ- transport depends on the coordinated interaction of photosys- ent plant ecosystems (6-8) and the fact that substantially tem II (PSH) and photosystem I (PSI) in the electron-transport different pigments absorb light for PSI and for PSII in the chain. Each photosystem contains distinct pigment-protein thylakoid membrane of oxygenic photosynthesis. complexes that harvest lightfrom different regions ofthe visible These findings suggested that higher plants and algae spectrum. The light energy is utilized in an endergonic electron- possess regulatory mechanisms that enable chloroplasts to transport reaction at each photosystem. Recent evidence has adjust and optimize the function of the light reactions under shown a large variability in the PSI/PSI stoichiometry in diverse conditions. Recently, evidence in the literature sug- plants grown under different environmental irradiance condi- gested long-term adjustments in photosystem stoichiometry tions. Results in this work are consistent with the notion of a as a plant response to different light-quality conditions during dynamic, rather than static, thylakoid membrane in which the stoichiometry of the two photosystems is adjusted and opti- growth (9, 10). Changes in photosystem stoichiometry, oc- mized in response to different light quality conditions. Direct curring in response to different light qualities, may be a evidence is provided that photosystem stoichiometry adjust- compensation reaction in the thylakoid membrane, serving to ments in chloroplasts are a compensation strategy designed to correct uneven absorption of light by the two photosystems. correct unbalanced absorption of light by the two photosys- However, the effect of these adjustments on the quantum tems. Such adjustments allow the plant to maintain a high yield of photosynthesis in higher plants has not been inves- quantum efficiency of photosynthesis under diverse light qual- tigated before. This work provides direct evidence that ity conditions and constitute acclimation that confers to plants adjustments of photosystem stoichiometry in chloroplasts a significant evolutionary advantage over that of a fixed permit the plant to retain a quantum efficiency of photosyn- photosystem stoichiometry in thylakoid membranes. thesis near the theoretical maximum. Energy transduction in photosynthesis depends on the coor- MATERIALS AND METHODS dinated electron turnover by two photosystems in a linear electron-transport process. Photosystem II (PSII) is involved Growth of Plants. Pisum sativum L. cv. Greenfeast was in a light-dependent oxidation of water and reduction of cultivated in a growth chamber under controlled conditions plastoquinone. Electrons from plastohydroquinone reach (18 hr of light at 240C/6 hr of dark at 140C). The growth light photosystem I (PSI) via the cytochrome b6-f complex and was either incandescent illumination filtered by red Plexiglas plastocyanin. PSI is involved in a light-dependent electron (PSI light; t75 umol of photons m-2-s-1; 580-740 nm), or transport to ferredoxin and to NADP'. Each photosystem is cool-white fluorescent illumination filtered by yellow Plexi- associated with distinct pigment-protein complexes, which glas (PSII light; -95 /Lmol of photons-m-2_s1l; 520-695 nm). absorb solar radiation and transfer excitation energy to the The relative intensity ofthe two light sources was selected so photochemical reaction center. that the integrated absorption of light by chloroplasts in the In almost every photosynthetic organism, light-harvesting leaves would be about the same under PSI-light and PSII- pigments of PSII are different from those of PSI, thus light conditions (11). The relative spectral irradiance of each allowing different wavelengths of light to sensitize the two growth-light regime, measured by a spectroradiometer photosystems unevenly. For example, wavelengths oflight in (SR3000A, Macam Photometrics, Livingston, Scotland), is the 600- to 650-nm region are absorbed preferentially by the shown in Fig. 1. Plants were harvested 20-22 days from phycobilins in cyanobacteria and red algae, or by chlorophyll sowing. To ensure sample uniformity, only the fourth pair of b in higher plant chloroplasts. These wavelengths oflight will leaflets from the base was harvested and used in this study. induce a faster electron turnover at PSI1 than at PSI. On the Assay of Thylakoid Membrane Components. Chloroplasts other hand, wavelengths of light absorbed primarily by were isolated (12) and stored at 77 K until use. Chlorophyll chlorophyll a and 8-carotene will induce a faster electron concentration was determined in 80% acetone (13) using a turnover at PSI than at PSII (1). Hitachi (Tokyo) model U-3300 spectrophotometer. The con- The quantum yield ofphotosynthesis in many species from centration ofcytochromefwas determined (14) with a Hitachi diverse light habitats is -0.106 + 0.001 mol of02 evolved per 557 double-beam spectrophotometer. The concentration of mol of photon absorbed (2-5). This value is very close to a PSII reaction centers was estimated from the number of theoretical upper limit of 0.125 mol of 02 evolved per mol of 3'-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU)-binding photon absorbed, translating to a photosynthesis efficiency sites in the thylakoid membrane (12, 15). The concentration of of -85%, independent of the light climate in which plants PSI reaction centers was estimated from the light-induced grow. This is a remarkable feature of the photosynthetic absorbance change at 703 nm (12, 16). The publication costs of this article were defrayed in part by page charge Abbreviations: PSI, photosystem I; PSII, photosystem II; DCMU, payment. This article must therefore be hereby marked "advertisement" 3'-(3,4-dichlorophenyl)-1,1-dimethylurea. in accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 7502 Downloaded by guest on September 28, 2021 Botany: Chow et al. Proc. Natl. Acad. Sci. USA 87 (1990) 7503 responses of the photosynthetic apparatus to the resulting long-term imbalance in light absorption by the two photo- 0 2 PSI- light systems, we measured the chlorophyll content of leaves, the chlorophyll a/b ratio, and the concentrations of cytochrome f, PSII, and of PSI in the thylakoid membrane. 16, ~~PS11- light Pea plants acclimated to PSI light conditions had =413 Aumol of chlorophyll per m2 of leaf area, compared with 555 >. pumol of chlorophyll per m2 in the leaves of PSII light-grown plants (Table 1). The greater chlorophyll content per leaf area in PSII than in PSI light-grown plants could not be attributed to the differential rate of light absorption by the two photo- 0 systems (18). It probably reflects a differential activation of 500 600 700 phytochrome and/or of a blue light receptor that has resulted Wavelength (nm) in dissimilar leaf thickness and dissimilar chloroplast density in the cells ofthe two pea samples. Moreover, the chlorophyll FIG. 1. Spectral distribution of irradiance in each growth light a/b ratio ofthylakoids isolated from plants grown in PSI light environment, designed to favor excitation of one photosystem over (PSI light thylakoids) was lower compared with that of PSII the other. light thylakoids. These results indicated differences in the pigment composition of the leaves and/or in the relative Leaf Photosynthesis Measurements. Rates of 02 evolution amount of PSII and PSI units in the thylakoid membrane of at 25°C and =1% C02/99% air were measured with a Han- the two samples (19-21). However, on a chlorophyll basis, satech (Kings Lynn, U.K.) leaf disc oxygen electrode (17). the concentration of cytochrome f, and therefore the cy- Actinic light for these measurements was provided by a tochrome b6-fcomplex, was essentially the same in PSI and quartz halogen light bulb. The white light was filtered to give PSII light thylakoids (Table 1). a predominantly PSI or PSII irradiance. PSI irradiance was Quantitation of reaction centers was obtained from the obtained by passing the white actinic light through red number of DCMU-binding sites (PSII measurement) and Plexiglas (Rohm and Haas, no. 2423). PSII irradiance was from the amount ofphotooxidizable P700 (PSI measurement) obtained by a combination of yellow Plexiglas (Rohm and in isolated thylakoid membranes (16, 22). Table 1 shows that Haas, no. 2208) and a long-wavelength cut-off filter [Ealing PSI light thylakoids had a greater number of DCMU-binding (Holliston, MA), 35-5453 VIQ 5-8]. The predominantly PSI sites (greater PSII reaction center concentration) per unit of or PSII irradiance for the measurement of 02 evolution was chlorophyll, compared with PSII light thylakoids. In contrast similar to the respective PSI and PSII light conditions used to the results from the PSI1 assay, the concentration of for plant growth (Fig. 1). The
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