JXB Advance Access originally published online on March 29, 2005
Journal of Experimental Botany 2005 56(416):1517-1523; doi:10.1093/jxb/eri147
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RESEARCH PAPER |
The stoichiometry and antenna size of the two photosystems in marine green algae, Bryopsis maxima and Ulva pertusa, in relation to the light environment of their natural habitat
Department of Biology, Faculty of Science, Toho University, Miyama 2-2-1, Funabashi, Chiba 274-8510, Japan
* To whom correspondence should be addressed. Fax: +81 47 472 5330. E-mail junya{at}bio.sci.toho-u.ac.jp
Received 23 November 2004; Accepted 28 February 2005
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Abstract |
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The stoichiometry and antenna sizes of the two photosystems in two marine green algae, Bryopsis maxima and Ulva pertusa, were investigated to examine whether the photosynthetic apparatus of the algae can be related to the light environment of their natural habitat. Bryopsis maxima and Ulva pertusa had chlorophyll (Chl) a/b ratios of 1.5 and 1.8, respectively, indicating large levels of Chl b, which absorbs blue-green light, relative to Chl a. The level of photosystem (PS) II was equivalent to that of PS I in Bryopsis maxima but lower than that of PS I in Ulva pertusa. Analysis of QA photoreduction and P-700 photo-oxidation with green light revealed that >50% of PS II centres are non-functional in electron transport. Thus, the ratio of the functional PS II to PS I is only 0.46 in Bryopsis maxima and 0.35 in Ulva pertusa. Light-response curves of electron transport also provided evidence that PS I had a larger light-harvesting capacity than did the functional PS II. Thus, there was a large imbalance in the light absorption between the two photosystems, with PS I showing a larger total light-harvesting capacity than PS II. Furthermore, as judged from the measurements of low temperature fluorescence spectra, the light energy absorbed by Chl b was efficiently transferred to PS I in both algae. Based on the above results, it is hypothesized that marine green algae require a higher ATP:NADPH ratio than do terrestrial plants to grow and survive under a coastal environment.
Key words: Antenna size of PS I and PS II, Bryopsis maxima, light environment, PS II:PS I ratio, marine green algae, Ulva pertusa
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Photosynthetic electron transport involves two photosystems: photosystem (PS) II which transfers electrons from water to the plastoquinone pool, and PS I which mediates electron transfer from the plastoquinone pool to NADP+. Thus, balance in the light absorption between the two photosystems is important for the operation of the photosynthetic apparatus with high efficiency. The antenna of each photosystem in higher plants and green algae consists of chlorophyll (Chl) a, Chl b, and carotenoids that bind to the reaction centre complex and the light-harvesting Chl–protein complex. The reaction centre complexes of PS I and PS II carry about 100 and 50 Chl a molecules, respectively. The major light-harvesting Chl–protein, LHC II, that preferentially transfers excitation energy to the PS II reaction centre, carries about 50% of the Chl and most of the Chl b molecules.
The stoichiometry and antenna size of the two photosystems alter under different growth light conditions. Shade plants or plants grown in low light have higher levels of LHC II and hence larger antenna sizes of PS II and lower Chl a/b ratios than do sun plants or plants grown in high light (Melis and Harvey, 1981
; Leong and Anderson, 1984; De la Torre and Burkey, 1990; Melis, 1991). The PS II:PS I ratio increases when plants are grown in light that selectively excites PS I and decreases in plants that receive light that is preferentially absorbed by PS II during growth (Melis and Harvey, 1981; Kim et al., 1993; Walters and Horton, 1994; Murchie and Horton, 1998). These observations show that plants have an ability to adjust the PS II:PS I ratio and antenna size of the two photosystems in response to the quantity and spectral quality of light to which plants are exposed during growth.
It is well known that irradiance sharply decreases with increasing depth of seawater, accompanied by marked changes in the spectral quality of light due to selective attenuation of red and blue light (Takahashi et al., 1989), although in some oceanic regions seawater does not show these spectral changes. The Chl a/b ratio of marine green macro-algae, almost all of which are members of Ulvophyceae, falls within the unusually low range of about 1.5–2.2 (Nakamura et al., 1976; Anderson et al., 1980; Nakayama and Okada, 1990), compared with about 3.0 in C3 sun plants (Melis, 1991). Thus, the algae are relatively abundant in Chl b, which absorbs green light more effectively on a per mole pigment basis than does Chl a. Further, the siphonous green algae also possess two unique xanthophylls, siphonaxanthin and siphonein, that have main absorption bands between 500 and 550 nm. The pigment composition of marine green algae is considered to have adapted well to the light environment of their natural habitats, which are rich in green or blue-green light (Yokohama et al., 1977; Anderson, 1983).
Little is known about photosystem stoichiometry and its relationship to the coastal marine environment. In the present study, the photosynthetic organization of two marine green algae, Bryopsis maxima and Ulva pertusa, that inhabit sea coasts, was investigated. Levels of PS I and PS II, as well as the light-harvesting capacities, of the two photosystems were determined to examine the balance in the light absorption between the two photosystems. The excitation spectra for fluorescence emitted from PS I and PS II were measured to determine pigments that serve as antennae for the two photosystems. The results are discussed in consideration of the physical and chemical environments of the natural habitat of the algae.
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Materials and methods |
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Sample collection and thylakoid membranes preparation
Bryopsis maxima and Ulva pertusa were collected from the sandy coast of Kimigahama in Choshi City, Chiba Prefecture (35°42' N, 140°52' E). The sampling site is a rocky area along the coast of the Pacific Ocean, and has a mean tide level of 1.5 m from December to April, when B. maxima and U. pertusa grow. Since the ebb tide occurs at midnight during the growth period, the two algae inhabit a depth of about 3 m during the day to avoid the strong waves. Plants were collected at midnight and transferred to the laboratory in a dark container.
Intact chloroplasts were prepared from B. maxima as described previously (Katoh et al., 1975). The intact chloroplasts can be prepared from B. maxima quickly and very gently, since the cell content is readily released by gently squeezing the segments of the coenocytic cellular organization. In brief, pinnate thalli were cut into small segments and the cell sap was squeezed through four layers of gauze into a medium that contained 10 mM HEPES–NaOH (pH 7.4), 1 M sorbitol, 2 mM NaCl, 2 mM MgCl2, and 1 mM EDTA. Chloroplasts were collected by fractional centrifugation, then washed once with and suspended in the preparation medium. Thylakoid membranes were prepared by osmotically disrupting chloroplasts with 10 mM HEPES–NaOH (pH 7.4) for 30 min at 0 °C and collected by centrifugation at 38 000 g for 30 min. The hypotonic treatment was repeated three times, removing white starch grains at the bottom of the tubes after each centrifugation.
For preparation of thylakoid membranes from U. pertusa, the laminar thalli were homogenized with a Waring blender in the preparation medium described above. After passing through four layers of gauze, the homogenate was centrifuged at 250 g for 15 min and thylakoid membranes were recovered from the supernatant by centrifugation at 15 000 g for 15 min and suspended in the medium. Chloroplasts and thylakoid membranes were quickly frozen in liquid nitrogen and stored at –85 °C until use.
Determination of electron transport components
Determinations of P-700 and cytochrome (Cyt) f content were measured according to Yamazaki et al. (1999). Levels of C-550 as PS II reaction centre were quantified according to the method described in Yamazaki et al. (1999), but with slight modifications. The light-induced absorbance change of C-550, an electrochromic band shift of pheophytin that is associated with QA (the primary quinone electron acceptor in PS II) photoreduction, was determined at 550 nm with a reference wavelength at 540 nm. Red actinic light was obtained by passing light through a 650 nm interference filter, with the photomultiplier guarded by a CS 4-96 filter. The differential absorption coefficient used was 5.2 mM–1 cm–1 (Yamazaki et al., 1999). Thylakoid membranes were treated with 0.2% (w/v) dodecyl-ß-D-maltoside at 0 °C for 60 min, and the supernatant obtained by centrifugation at 10 000 g for 5 min was used for measurement. The detergent-treatment greatly diminished light-scattering of samples without any appreciable effects on light-induced spectral changes. The reaction was carried out in medium containing 50 mM HEPES–NaOH (pH 7.4), 10 mM NaCl, and 5 mM MgCl2, to which 4 mM ferricyanide, 10 µM 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU), 20 µM gramicidin D, 0.04% (w/v) dodecyl-ß-D-maltoside, and the membrane fragments equivalent to 75 µg Chl ml–1 were added. The level of Chl was determined spectrophotometrically by the method of Porra et al. (1989).
Measurement of antenna size of PS I and PS II
Relative antenna sizes of PS I and PS II were determined by measuring rate constants of P-700 and QA photoreduction, respectively, according to Yamazaki et al. (1999). For measurement of P-700 photoxidation, a red cut-off filter (R-66; Toshiba, Japan) was inserted between the cuvette and the photomultiplier to remove scattered actinic light. The two types of PS II reaction centres, the PS II
and the PS IIß centres, were estimated by analysing the area over the fluorescence induction curves in the presence of DCMU as described in Melis and Homann (1975, 1976). Thylakoid membranes (30 µg Chl ml–1) and 20 µM DCMU were added to the basal medium. Photoreduction of QA was analysed by measuring the growth of a complementary area over the fluorescence induction curve with a custom-made apparatus (Yamazaki et al., 1999). Thylakoid membranes containing 6–10 µg Chl ml–1 were suspended in 50 mM HEPES–NaOH (pH 7.4), 10 mM NaCl, 5 mM MgCl2, 0.4 M sucrose, and 20 µM DCMU.
Measurement of electron transport activities
Electron transport activities of PS I and PS II were determined with a Clark-type oxygen electrode at 25 °C. The light source was a halogen lamp and light intensity was varied with neutral density filters. A Li-Cor photon sensor (Model LI-183) was used to monitor photon flux density. The composition of the basal medium was 50 mM HEPES–NaOH (pH 7.4), 0.4 M sucrose, 10 mM NaCl, and 5 mM MgCl2. For measurement of PS I electron transport, the medium was supplemented with 1 mM methyl viologen, 0.5 mM 2,6-dichlorophenolindophenol, 2 mM sodium ascorbate, 1 µM gramicidin D, and 10 µM DCMU. PS II electron transport activity was determined in the presence of 1 mM phenyl-p-benzoquinone, 1 µM gramicidin D, and 0.5 µM 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone. The concentration of chloroplasts or thylakoid membranes was 20 µg Chl ml–1.
Measurement of 77K fluorescence spectra
For the low-temperature fluorescence emission and excitation spectra, the thylakoid membranes (100 µg Chl ml–1) were suspended in 50 mM HEPES–NaOH (pH 7.4), 10 mM NaCl, 5 mM MgCl2, and 0.4 M sucrose. A sample was placed in a custom-made sample holder, and the holder was submerged in liquid nitrogen. The excitation and the emission slit were set at 5.0 nm. For the measurement of the emission spectra, the excitation wavelength was set at 440 nm and the emission wavelength was stored in a computer from 600 to 800 nm at 0.5 nm intervals. For the measurement of the excitation spectra, the emission wavelength was set at 685, 695, and 720 nm and the excitation wavelength was stored in a computer from 400 to 600 nm at 0.5 nm intervals.
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Results |
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Thylakoid components in B. maxima and U. pertusa
The Chl a/b ratios and levels of the thylakoid components related to electron transport in the marine green algae B. maxima and U. pertusa were determined, and the results are summarized in Table 1. Both algae had low Chl a/b ratios (Table 1). This finding was in agreement with earlier observations that marine green algae have more Chl b relative to Chl a than do terrestrial C3 plants, which have Chl a/b ratios of about 3 (Nakamura et al., 1976
; Anderson et al., 1980; Anderson, 1983; Nakayama and Okada, 1990). As shown in Table 1, B. maxima had nearly equal levels of the two photosystems, while the level of PS II was lower than that of PS I in U. pertusa. The PS II:PS I ratios of C3 sun plants and several unicellular green algae have been reported as 1.7 and about 1.4, respectively (Melis, 1991). Thus, the algae have smaller PS II:PS I ratios, which implies that their two photosystems—and especially PS II—have larger antenna sizes than those of terrestrial plants. The levels of Cyt f are presented in Table 1, along with the resulting Cyt f:PS I ratios of 0.97 in B. maxima and 1.45 in U. pertusa.
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PS II heterogeneity and light absorption balance in B. maxima and U. pertusa
PS II is heterogeneous, and fluorescence induction in the presence of DCMU was analysed to distinguish between the PS II
centre, which is functional in electron transport, and the PS IIß centre, which is non-functional in QB (the secondary quinone electron acceptor in PS II) reduction or linear electron transport (Melis and Homann, 1975, 1976; Lavergne, 1982). As shown in Table 2, the PS II centre accounted for <50% of the total PS II centres in both algae. Thus, when the active PS II centres are taken into account, large imbalances occur between the two photosystems, the PS II:PS I ratio being 0.46 in B. maxima and 0.35 in U. pertusa.
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It is possible that PS II has a larger antenna size than PS I, and thus light absorption between the two photosystems is balanced in spite of the low PS II
:PS I ratios.
Antenna size of the two photosystems in B. maxima and U. pertusa
Two approaches were taken to assess the antenna size of the two photosystems. First, the relative antenna sizes of the two photosystems were determined by measuring the steady-state rate of electron transport. Figure 1 shows the light-response curves of the electron transport mediated by PS I or PS II alone, which are normalized at the maximum rates attained. Unexpectedly, the initial slope of the light-response curves of PS I electron transport was steeper than that of PS II electron transport. When an equal quantum efficiency is assumed for the two photosystems, the initial slope of the light-response curve is a measure of the light-harvesting capacity. Thus, the result is consistent with the notion that PS I has a larger antenna size than does the functional PS II in the two algae.
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Second, the antenna sizes of the PS I and PS II centres were estimated by measuring the rates of P-700 photooxidation and QA photoreduction (Table 2). The kinetics of P-700 photo-oxidation and QA photoreduction determined with green light of a limited intensity provided information about the relative antenna sizes of PS I and PS II, respectively (Melis, 1991
). The KI values thus determined indicate that Bryopsis PS I had a slightly larger antenna size than did Ulva PS I (Table 2).
The rate constant of QA photoreduction in PS IIß (Kß) is several times smaller than that in PS II (K), and this has been taken as evidence that PS IIß has a smaller antenna size than PS II (Melis, 1991). A previous report indicated that the rate constant of QA photoreduction is proportional to the antenna size of PS II (Yamazaki et al., 1999). In the present study, as shown in Table 2, K was significantly smaller than KI in both algae. It is unlikely that the low K values were a consequence of photoinhibition of PS II, because the two algae showed Fv:Fm (variable to maximum fluorescence) ratios of above 0.7, indicating that PS II was operating with high quantum efficiency. Therefore, the obtained rate constants can be considered to indicate that the functional PS II had a smaller antenna size than did PS I in the two algae. To date, low Chl a/b ratios have always been considered to indicate large antenna size in PS II. In these algae, however, the low Chl a/b ratios suggested large sizes of both PS I and LHC II antennae. Therefore, the following experiments were carried out to test this hypothesis.
77K fluorescence emission and excitation spectra in B. maxima and U. pertusa
In general, LHC II is the major light-harvesting Chl a/b–protein complex of PS II in the thylakoid membranes of higher plants and green algae and preferentially transfers excitation energy to PS II. This leads to a question: How is it that PS I has a larger antenna size than PS II? It is difficult to explain the larger antenna size of PS I unless it is assumed that a substantial amount of LHC II is contributed as an antenna to PS I.
If LHC II serves as an antenna of PS I, it would be expected that the light energy absorbed by Chl b would be efficiently transferred to PS I. Figure 2 shows the fluorescence emission spectra of isolated thylakoid membranes from the two algae that were determined at 77K. The low-temperature fluorescence emission spectrum of the Bryopsis thylakoid membranes had maxima at 685 and 695, and the PS I band appeared as a small shoulder at 718 nm (Fig. 2A). By contrast, that of the U. pertusa thylakoid membranes showed a prominent emission band at 720 nm that was well separated from the PS II fluorescence bands at shorter wavelengths (Fig. 2B).
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The excitation spectra of the three fluorescence bands are shown in Fig. 3. The excitation spectra for the 685 nm and 695 nm bands were similar, demonstrating that light absorbed by Chl a (438 nm), Chl b (470 nm), and the carotenoids (490 nm) were transferred to PS II (Fig. 3C–F). The spectrum of B. maxima additionally showed a band at 538 nm that has been ascribed to siphonaxanthin and siphonein (Anderson, 1983
; Nakayama and Okada, 1990). Note that the Chl b band at 470 nm and the xanthophyll band at 538 nm were more pronounced than the Chl a band at 438 nm, indicating that light energy absorbed by Chl b, siphonaxanthin, and siphonein was efficiently transferred to PS II (Fig. 3C, E). These results are consistent with the notion that LHC II serves as an antenna of PS II, because Chl b, siphonaxanthin, and siphonein are mostly located in LHC II, whereas a substantial fraction of Chl a is present in PS I complexes and LHC I.
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The excitation spectra for the 720 nm emission band also showed peaks or shoulders at 438, 470, and 490 nm that were absorbed by Chl a, Chl b, and the carotenoids, respectively (Fig. 3A, B). The spectrum of B. maxima, with its pronounced 470 nm band, resembled the excitation spectra for the emission bands from PS II. This suggests that the emission band at 720 nm might include a large contribution from PS II in this alga, and thus that LHC II makes equal contributions to the light-harvesting of PS I and PS II. Furthermore, siphonaxanthin and siphonein also served as antenna pigments of PS I (Fig. 3A). By contrast, the contribution from PS II should be minimal in U. pertusa, where the 720 nm emission band was well separated from the emission bands of PS II (Fig. 2B). Although the excitation spectrum for the 720 nm band also indicates that Chl b functions as an antenna in PS I, the 470 nm band was lower than the Chl a band at 438 nm (Fig. 3B). This difference may be ascribed to the fact that PS I, which has a larger-size Chl a antenna than PS II, is more abundant than PS II in U. pertusa. The results suggest that a substantial part of the LHC II fraction serves as an antenna of PS I in marine green algae.
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Discussion |
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The two marine green algae, B. maxima and U. pertusa, have lower Chl a/b ratios, larger numbers of Chl molecules per PS I or PS II reaction centre, and lower PS II:PS I ratios compared with terrestrial vascular plants (Table 1). These features of the two marine green algae are reminiscent of those of low-light plants or shade plants, which have higher levels of LHC II, and hence lower Chl a/b ratios and larger antenna size of PS II, than do plants grown in high light (Melis and Harvey, 1981
; Leong and Anderson, 1984; De la Torre and Burkey, 1990; Melis, 1991). The difference between terrestrial plants and algae is ascribed to different Chl compositions of LHC II, because LHC II isolated from B. maxima carries six Chl a and eight Chl b molecules, in addition to three molecules of siphonaxanthin and one each of siphonein and neoxanthin (Nakayama et al., 1986), resulting in a Chl a/b ratio of about 0.8 (Table 1; see Nakayama et al., 1986). Reductions in the PS II:PS I ratio or Cyt f:PS I ratio to below 1.0 have been reported for several vascular plants that were grown in low light (Leong and Anderson, 1984; De la Torre and Burkey, 1990; Melis, 1991; Yamazaki et al., 1999). Furthermore, the increased level of Chl b and the occurrence of siphonaxanthin and siphonein are advantageous for the two algae because the underwater light environment is rich in green light. Thus, the photosynthetic apparatus of the two algae can be related to the light environment of their native habitat.
An unexpected observation was that PS I was present in large excess over the functional PS II in the marine green algae (Fig. 1; Table 2). However, the present analysis of the growth of the complementary area over the fluorescence induction curve indicated that >50% of the PS II centres were inactive in the electron transport (Table 2). There was a greater abundance of PS I than of functional PS II in both algae, although the actual percentage of the inactive PS II centre determined by this procedure must be taken with some reservations (Krause and Weis, 1991; Yamazaki et al., 1999). Moreover, the kinetics of P-700 photo-oxidation and QA photoreduction showed that PS I has a larger antenna size than does PS II (Table 2).
If PS II shows a larger light-harvesting capacity than does PS I in the habitat of all algae, the light absorption between the two photosystems would be balanced so as to enable algae to perform photosynthesis with high efficiency. The initial slope of the light-response curve also provided evidence for a larger light-harvesting capacity in PS I than in PS II (Fig. 1). Therefore, the total antenna size of PS I exceeds that of PS II in both algae.
This unexpected observation is difficult to explain unless LHC II serves as an antenna of PS I. In fact, the excitation spectra for fluorescence emissions from PS I and PS II showed that light energy absorbed by Chl b and the carotenoids, siphonaxanthin and siphonein, was efficiently transferred to PS I (Fig. 3A, B). Because the major portion of Chl b and the two carotenoids is located in LHC II, these observations propose that a substantial fraction of LHC II is able to transfer excitation energy very efficiently to PS I in the marine green algae.
However, the question that must be raised is: Why does the antenna size of PS I exceed that of PS II? To answer this question, it is possible to establish a working hypothesis about the function of PS I. There is evidence that PS I energizes the light-induced active transport of substances in algae (Wiessner, 1965; Kandler and Tanner, 1966). It is speculated that the involvement of a cyclic photophosphorylation produces a larger amount of ATP than that produced by terrestrial plants or freshwater algae as energy to import various nutrients. Cyclic photophosphorylation is enhanced by increasing the Na concentration in the reaction medium (Murakami et al., 1997), and by cellular growth under a low CO2 condition, which causes an increased need for ATP generation in the cells in order to meet the requirements of 
active transport (Manodori and Melis, 1984). In addition, there are large gradients of Na+, K+, and other ions across the plasmalemma in marine green algae (Ritchie, 1988). Furthermore, since the habitat of these algae is enriched in blue-green light, light energy absorbed by Chl b and the carotenoids is preferentially transferred to LHC II, with the result that PS II undergoes a state transition to state II; the state transition is a mechanism to balance light utilization between the two photosystems (Horton et al., 1996). Because cyclic electron transport is active in state II, a high rate of ATP synthesis occurs (Finazzi et al., 2001), with the result that large amounts of ATP are consumed to maintain the physiological concentrations of ions in the cytosol and vacuoles of marine algae.
The present study revealed that there is a large imbalance in light absorption between the two photosystems in both B. maxima and U. pertusa. Because PS I mediates cyclic photophosphorylation, the implication is that the marine green algae require a higher ATP:NADPH ratio for growth and survival than do terrestrial plants. Furthermore, it is possible that the imbalance in the photosystem stoichiometry protects these algae and perhaps other marine organisms from photoinhibition in light that preferentially excites PS II.
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Acknowledgements |
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We would like to express our gratitude to our laboratory collaborators for excellent technical assistance and continuous encouragement the course of this work.
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Footnotes |
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Abbreviations: LHC I and LHC II, light-harvesting chlorophyll a/b-protein complexes associated with PS I and PS II, respectively; P-700, photochemical reaction centre of photosystem I; QA, the primary quinone electron acceptor in photosystem II; QB, the secondary quinone electron acceptor in photosystem II.
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