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1 Plant CellPhysiol. 37(3): (1996) JSPP 1996 Antenna Sizes of Photosystem I and Photosystem II in Chlorophyll b- Deficient Mutants of Rice. Evidence for an Antenna Function of Photosystem II Centers That are Inactive in Electron Transport Tomio Terao ' and Sakae Katoh 2 1 Biological Resources Division, Japan International Research Center for Agricultural Sciences, 1-2 Ohwashi, Tsukuba, Ibaraki, 305 Japan 2 Department of Biology, Faculty of Science, Toho University, Miyama, Funabashi, 274 Japan Light-harvesting capacities of photosystem I (PSI) and photosystem II (PSII) in a wild-type and three chlorophyll 6-deficient mutant strains of rice were determined by measuring the initial slope of light-response curve of PSI and PSII electron transport and kinetics of light-induced redox changes of P-700 and Q A, respectively. The light-harvesting capacity of PSI determined by the two methods was only moderately reduced by chlorophyll 6-deficiency. Analysis of thefluorescenceinduction that monitors time course of Q A photoreduction showed that both relative abundance and antenna size of PSII a decrease with increasing deficiency of chlorophyll b and there is only PSII,, in chlorina 2 which totally lacks chlorophyll b. The numbers of antenna chlorophyll molecules associated with the mutant PSII centers were, therefore, three to five times smaller than that of PSII a in the wild type rice. Rates of PSII electron transport determined on the basis of PSII centers in the three mutants were 60-70% of that in the normal plant at all photon flux densities examined, indicating that substantial portions of the mutant PSII centers are inactive in electron transport. The initial slopes of light-response curves of PSII electron transport revealed that the functional antenna sizes of the active populations of PSII centers in the mutants correspond to about half that of PSII a in the wild type rice. Thus, the numbers of chlorophyll molecules that serve as antenna of the oxygen-evolving PSII centers in the mutants are significantly larger than those that are actually associated with each PSII center. It is proposed that the inactive PSII serves as an antenna of the active PSII in the three chlorophyll ^-deficient mutants of rice. In spite of the reduced antenna size of PSII, therefore, the total light-harvesting capacity of PSII approximately matches that of PSI in the mutants. Key words: Antenna size Chlorophyll ^-deficiency In- Abbreviations: LHC-I and LHC-II, light-harvesting Chi a/bproteins of PSI and PSII, respectively; Q A and Q B, primary and secondary quinone acceptor of PSII, respectively; DCIP, 2,6-dichlorophenolindophenol; DBMIB, dibromomethyl-isopropyl-pbenzoquinone; PSII a and PSII^, PSII centers with a large and a small antenna size, respectively; KI, K a and K^, rate constants of P-700 oxidation in PSI and Q A reduction in PSII a and PSII^, respectively; NIJ/I, total antenna size of PSII relative to PSI. active PSII Photosynthesis Rice. The stoichiometry of PSI and PSII and the functional state of PSII in Chi ^-deficient mutants of rice were investigated in the preceding paper (Terao et al. 1996). The PSII to PSI ratio is maximally 1.3 in the wild type rice cultivar, Norin No. 8, but increases to 1.8 in chlorina 2, a Type I mutant which totally lacks Chi b, and to 2 to 3 in two Type II mutants, chlorina 11 and chlorina 14, which have Chi a/b ratios of 9 and 13, respectively. The mutants are strongly deficient in LHC II (Terao et al. 1985b, Terao and Katoh 1989) and hence have reduced light-harvesting capacities of PSII. The elevated PSII to PSI ratios are, therefore, considered to be a response of the plant to reduce imbalance in light absorption between PSI and PSII. Measurement of oxygen evolution with repetitive flashes revealed, however, that, whereas maximally 20% of PSII centers are inactive in electron transport in the wild type plant, the inactive population amounts to about 50% of the total PSII in the mutant strains. Thus, when only the active PSII is taken into account, there is a notable imbalance in the light harvesting capacity between the two photosystems of the mutants. In the present study, we report that the inactive PSII centers serve as an antenna of the active PSII centers so that there is balance in light absorption between the two photosystems in the Chi fe-deficient mutants of rice. The light-harvesting capacity of PSII was determined by two different approaches. The functional antenna sizes of the active PSII centers were estimated from the initial slope of light-respose curve of oxygen evolution, whereas the numbers of Chi molecules associated with PSII centers were determined by analyzing the fluorescence induction which monitors time courses of Q A photoreduction. Light-harvesting capacities of PSI were also determined by measuring the initial slope of light-reponse curve and time corses of P-700 photooxidation and balance of light absorption between the two photosystems was estimated. 307

2 308 T. Terao and S. Katoh Materials and Methods Thylakoid membranes were prepared from 30-days old seedlings of rice (Oryza sativa L. cv. Norin No. 8) and the three chlorina mutants derived from the cultivar as described previously (Terao et al. 1985a). Evolution or uptake of oxygen was determined with a Clarktype oxygen electrode. Whole chain electron transport (PSI plus PSII) was assayed in a medium containing 50 mm Tricine-NaOH (ph 7.8), 2 mm MgCl 2, 10 mm NaCl, 0.2 mm methyl viologen, 2 mm NaN 3, 20 mm methylamine and 0.4 M sucrose. For assay of PSI electron transport, 1 fim DCMU, 5 mm ascorbate and 0.2 mm DCIP were added to the above medium. PSII electron transport was determined in the presence of 50 mm HEPES-NaOH (ph 7.0), 2 mm MgCl 2, 10 mm NaCl, 0.4 mm phenyl-p-benzoquinone, 1 mm potassium ferricyanide, 10 mm methylamine, 2 /JM DBMIB and 0.4 M sucrose. The concentration of Chi determined according to the method of Arnon (1949) was loji/g ml" 1. Samples were illuminated with white light from a halogen lamp and photon flux density was varied with neutral density filters. Relative antenna size of PSI was determined by analyzing time courses of P-700 photooxidation. The data obtained from 8 to 12 measurements were stored in a transient recorder and averaged with a computer. Green actinic light passed through a CS 4-96 filter and a 560 nm interference filter (15.2^mol photons m~ 2 s~'). Reaction mixture contained 50 mm HEPES-KOH (ph 7.0), 5 mm MgCl 2, 10 mm NaCl, 0.4 M sucrose and 50 fig Chi ml" 1. Time courses of the fluorescence induction were monitored as described in the preceding paper (Terao et al. 1996). Excitation light was the same as that used for measurement of P-700 photooxidation, except that photon flux density was 32.5//Em~ 2 s~'. Thylakoid membranes (50/ig Chi ml" 1 ) were suspended in the medium described above, to which 10/iM DCMU and 2 mm ferricyanide were supplemented. Results Antenna size of PSI Relative antenna sizes of PSI in the wild-type and three Chi 6-deficient mutant strains of rice were estimated by two different methods. First, electron transport from DCIPH 2 to methyl viologen was measured at different photon flux densities. As shown in Fig. 1A, rates of PSI electron transport determined on the basis of Chi were highest in chlorina 2 at all the photon flux densities examined and decreased in the order of the two Type II mutants and the wild-type rice. The differences are ascribed to the reduced Chi contents of the mutant genotypes (Terao et al. 1988). When the rates of electron transport are replotted against the PSI contents determined by P-700 photooxidation, the differences in the light-response curves among the four genotypes largely disappeared (Fig. IB). This indicates that rate of PSI electron transport from DCIPH 2 to methyl viologen is determined by the concentration of P-700, or plastocyanin which is present at a stoichiometric ratio to P-700. The initial slope of the curve is linearly related to the antenna size of PSI, when the quantum efficiency of PSI is assumed not to be affected by the Chi ^-deficiency. Relative antenna sizes of PSI determined for the four genotypes are shown in Table 1. The light-harvesting capacity of PSI in the mutants are only 10 to 20% smaller than that in the wild-type rice. The second approach used for estimation of the antenna size of PSI was kinetical analysis of P-700 photooxidation. When reduction of P with electrons from the intersystem electron carriers had been blocked by inactivating plastocyanin with KCN (Izawa et al. 1973, Melis 1982), P-700 was photooxidized with the first order reaction kinetics in all the genotypes (not shown). At the limiting photon flux density employed, rate constant of P-700 photooxidation (KI) is a measure of the antenna size of PSI (Melis 1982). The KI values obtained are shown in Table B 140 Q. O 120 & Incident photon flux density ( >. > I9 c7. ) ? Photon flux density (uenri^s" 1 ) Incident photon flux density 8000 Fig. 1 Dependence upon photon flux density of rates of PSI electron transport determined on the basis of Chi (A) and P-700 (B) in the wild-type and three chlorina mutant strains. Inset, initial slopes of the light-response curves normalized at maximum rates. Closed circles, Norin No. 8; open circles, chlorina 2; triangles, chlorina 11; squares, chlorina 14.

3 Antenna sizes of PSI and PSII 309 Table 1 Relative antenna sizes of PSI and PSII estimated from the initial slopes of light-response curves of electron transport in the wild-type and three mutant strains Norin No. 8 Chlorina 2 Chlorina 11 Chlorina 14 PSI PSII Relative antenna size of PSI was reduced by 26% in chlorina 2 and in lesser extents in chlorina 11 and chlorina 14 by the deficiency of Chi b. Thus, the two approaches show a minor contribution of LHC-I to the PSI antenna. The antenna size of PSI in the Chi Wess chlorina f2 mutant of barley has been shown to be 20% smaller than that of PSI in the wild type plant (Ghirardi et al. 1986). Antenna size of PSII Light-harvesting capacity of PSII was evaluated by analyzing kinetics of Q A photoreduction in the presence of DCMU. Time courses of Q A reduction were monitored through the growth of a complementary area over the fluorescence induction curve (Melis and Homann 1975). The semilogarithmic plot of the area growth showed two kinetical components in the normal thylakoids. A fast sigmoidal component and a slow exponential component are ascribed to PSII a and PSII^, respectively. PSII a and PSILj corresponded to 70% and 30% of the PSII reaction centers, respectively (Table 2). The rate constants of Q A reduction in PSII O (KJ and PSII^ (K^) are related to the antenna sizes of the two centers. K a was 5.3 times larger than K fi. Chlorina 11 and chlorina 14 also showed a heterogeneity of PSII. Reflecting low contents of LHC-II, however, PSII^ was more abundant than PSII O in the two mutants. K a was also reduced by the Chi 6-deficiency, whereas K^ remained essentially unaltered. The heterogeneity of PSII was not apparent in chlorina 2; when photoreduction of Q A was approximated by the first order kinetics, a rate constant similar to K^ of other strains was obtained. Thus, the Chi b deficiency reduces the light-harvesting capacity of PSII by decreasing both relative abundance and antenna size of PSII 0. Based upon the KI, K a and K^ values estimated above and the contents of PSI and PSII determined in the preceding paper (Terao et al. 1994), the numbers of Chi molecules that function as antenna of respective PSII centers were estimated (Melis 1990). The antenna sizes of PSI are 120 to 157 Chi per center in the four genotypes. The antenna Chi numbers of PSII a are 300 in the wild-type, 120 in chlorina 11 and 84 in chlorina 14, whereas that of PSII^ varies only in a narrow range of 56 to 74. Light-harvesting capacity of PSII was also determined by measuring light-response curves of oxygen evolution. The activity determined on the basis of Chi was higher in the mutants than in the wild type rice (not shown). In Fig. 3A, rates of oxygen evolution are plotted against the total PSII centers that were estimated from the magnitudes of Q A photoreduction at 325 nm (Terao et al. 1996). Note that the oxygen-evolving activities of the three mutants were 60-70% of that of the wild type rice at all photon flux densities examined. The preceding paper showed that about 50% of PSII centers are functional in electron transport in the three mutants, whereas the proportion of the active centers is 80% or more in the normal plant (Terao et al. 1996). When the data were replotted versus the active Table 2 Rate constants of P-700 photooxidation (KI) and Q A photoreduction in PSII a (K<J and PSII^ (K p ) and relative abundances of PSII a and PSUp in the wild-type and three mutant strains Norin No. 8 Chlorina 2 Chlorina 11 Chlorina 14 Rate constant KI K q Abundance PSII O PSII, (s- 1 ) The rate constants were corrected for intensity of actinic light. (s-) (s-) (s-)

4 310 T. Terao and S. Katoh \ \ Time (s) Norin No.B o chlorina 2 A chlorina 11 a chlorina 14 the percent distribution of Chi among Chl-proteins; LHC- II accounts for about 50% of the total Chi present in the thylakoids and about 30% and 15% of Chi are associated with PSI reaction center complexes (plus LHC-I) and PSII reaction center complexes, respectively (Terao et al. 1985b). In chlorina 2, PSI: PSII a : PSII^= 1.0 : 0 : Thus, Nny^l.03. Chlorina 11 and chlorina 14 have PSI: PSII 0 : PSII^ ratios of 1.0 : 0.89 : 1.59 and 1.0 : 0.58 : 1.65, respectively. We obtain Nn/i=1.43 for chlorina 11 and 1.05 for chlorina 14. Thus, when the inactive PSII centers are assumed to serve as antenna of the active centers, the total light-harvesting capacity of PSII is comparable to that of PSI in the chlorina mutants. Fig. 2 Semilogarithmic plots of the growth of the complementary areas over the fluorescence induction curves (solid lines). Broken lines show time courses of changes in PSII a which were obtained by subtracting the /?-components from the overall time courses. Closed circles, Norin No. 8; open circles, chlorina 2; triangles, chlorina 11; squares, chlorina 14. populations of PSII, light-saturating rates of oxygen evolution in the three mutants became comparable to that in the wild-type strain (Fig. 3B). This result indicates that steady state oxygen evolution in saturating continuous light is supported only by the part of PSII centers that was shown to be inactive in electron transport in the preceding paper (Terao et al. 1996). The initial slope of the light-response curves is, therefore, a measure of the functional antenna size of the active PSII centers. The initial slope of the curve determined for chlorina 2 that contains only VSll fi was about half that for the normal plant (Fig. 3B and Table 1). Thus, the functional antenna size of the oxygen-evolving PSII in the mutants is significantly larger than the antenna size of PSIlp estimated by Q A photoreduction. The initial slopes of light-response curves also gave larger antenna sizes for the active PSII in chlorina 11 and chlorina 14 than did the fluorescence analysis even when all PSII a present in the mutants are assumed to be active in electron transport. We propose, therefore, that the inactive PSII centers present in the three chlorina mutants serve as an antenna of the active PSII centers. Balance of light absorption between PSI and PSII Based upon the antenna sizes of the two photosysterns obtained above and the abundances of PSII and PSI determined previously (Terao et al. 1996), the ratio of the total antenna size of PSII to that of PSI (N n /i) was estimated (Melis 1990). The quantum efficiencies of the two photosystems are assumed not to be affected by Chi 6-deficiency. The PSII contents used are those estimated from the magnitudes of Q A photoreduction (Terao et al. 1996). We obtained N 1I/I = 2.11 for the wild-type rice, where PSI: PSII 0 : PSII^= 1.0 : 0.9 : 0.4. The ratio is consistent with Discussion The reaction center of PSII is heterogeneous in terms of electron transport and antenna size in the normal and three mutant strains of rice. The present study confirms the previous observation that the mutant strains have larger populations of the inactive PSII compared with the wild type rice (Terao et al. 1996). Rates of oxygen evolution determined on the basis of the total PSII were substantially smaller in the mutants than in the wild type plant at all photon flux densities examined. When plotted against the populations of PSII centers that had been shown to be active in electron transport in the preceding paper (Terao et al. 1996), light-saturating rates of oxygen evolution became comparable among the four genotypes. This indicates that the large populations of inactive PSII centers present in the mutants are unable to contribute to steady state oxygen evolution in strong continuous light. Graan and Ort (1986) showed that the number of PSII centers determined from the flash yield of oxygen varies depending upon quinone acceptor used: dichloro-p-benzoquinone receives electrons from the PSII centers, either functional or non-functional in plastoquinone reduction, whereas dimethyl-p-benzoquinone reacts only with the functional centers. Our results suggest that phenyl-p-benzoquinone is unable to rapidly accept electrons from the inactive centers, irrespective of illumination conditions. Analysis of the fluorescence induction kinetics provides information about the number of antenna Chi associated with respective PSII centers, regardless of their functional states. In the wild-type plant, 70% of PSII is PSII a that has 300 antenna Chi and the remainder is PSIIyj with 56 antenna Chi. This result is compatible with the notion that PSII a is functional in electron transport (Melis 1985) because the major proportion of PSII centers is active in oxygen evolution in the normal rice (Terao et al. 1996). In the following, therefore, the antenna size of the active PSII in the wild type rice is assumed to be that of PSII a. The proportions of the active PSII are larger than those of PSII a in

5 Antenna sizes of PSI and PSII Incident photon flux density (we-nrf'-s" 1 ) Incident photon flux density (ue-m' 2 -s H ) Fig. 3 Dependence upon photon flux density of PSII electron transport determined on the basis of the PSII reaction center. A, the total PSII estimated from amplitudes of Q A photoreduction. B, the active PSII estimated from the flash yield of oxygen. Inset, initial slopes of the light curves normalized at maximum rates. Closed circles, Norin No. 8; open circles, chlorina 2; triangles, chlorina 11; squares, chlorina 14. the mutants; whereas 54% of PSII centers are active in electron transport in the three mutants (Terao et al. 1996), PSII a corresponds to only 36% and 26% of the total PSII in chlorina 11 and chlorina 14, respectively, and there is no PSII a in chlorina 2. Thus, the functional state of PSII is not related to association of LHC-II in the mutants. The antenna size of PSII^ in chlorina 2 is 66 Chi molecules per center. This agrees well with the Chl/Q A ratio of 57 in purified oxygen-evolving PSII preparation isolated from another rice mutant (chlorina 9) which totally lacks LHC-II (Shen et al. 1988). The antenna Chi number of the mutant PSII is, therefore, 4.5 times smaller than that of PSII a in the wild-type plant. In contrast, the initial slope of light-response curve shows that the functional antenna size of the oxygen-evolving PSII centers in the mutant corresponds to 45% of that of PSII 0 in the wild-type rice (Table 1). Thus, the number of Chi that functionally serves as antenna of the active population of PSII^ is 135, which is twice larger than the number of Chi that are actually associated with PSH^ in the mutant. Because the abundance of the inactive PSII centers is comparable to that of the active centers, it is concluded from the data that light energy absorbed by the inactive PSII is efficiently transferred to and utilized by the active PSII. The data consistent with this conclusion were obtained with the two Type II mutants. The initial slopes of light-response curves showed that the functional antenna sizes of the active PSII in chlorina 11 and chlorina 14 are about half that in the wild type rice. However, the numbers of antenna Chi determined by photoreduction of Q A are at most one thirds that of the normal plant. Recently, the fluorescence induction kinetics in the

6 312 T. Terao and S. Katoh three chlorina rice mutants derived from Norin No. 8 has been studied by Hsu and Lee (1995) with a different analytical procedure. The authors reported that the growth kinetics of the complementary area over the induction curve consists of three phases with different rate constants even in a Type I mutant (chlorina 7) that has no Chi b. The two minor phases with slower rate constants are ascribed to abnormal PSII centers, in which Q A reduction is limited something other than light absorption. Their data do not affect our conclusion that the inactive PSII serves as an antenna of the active PSII, however. The antenna sizes of the major normal PSII populations in the mutants are at most 20% of that in the wild type rice and hence correspond to less than half the functional antenna sizes of the oxygen-evolving PSII centers estimated for the corresponding or comparable mutants. The antenna function of the inactive PSII largely compensates the reduced light-harvesting capacity of the mutant PSII. Thus, the total light-harvesting capacity of PSII is roughly comparable to that of PSI in the three chlorina mutants. This contrasts to the wild type rice, where the total antenna Chi number of PSII is about twice as large as that of PSI (Terao et al. 1996). This imbalance is considered to be compensated by the spill-over of excitation energy from PSII to PSI (Murata 1969, Myers 1971), by a smaller integrated absorption of light by Chi b than by Chi a and high pigment concentrations in the grana stacks where PSII is located (Melis 1991). All these compensation mechanisms depend upon the presence of Chi b or LHC-II and hence should be mostly or totally non-functional in the Chi 6-deficient mutants. An equimolar distribution of Chi between the two photosystems is, therefore, important for efficient utilization of light in the mutants. In conclusion, our results suggest the occurrence of a substantial population of PSII centers which contribute to light-harvesting but not to electron transport in the three Chi ft-deficient mutant strains. An advantage of this organization of PSII is that, in spite of reduced levels of LHC-II, the mutants are able to balance both light absorption and electron flow between the two photosystems. Thus, the results obtained in the present and the preceding studies (Terao et al. 1996) suggest that plants have a plasticity to adjust, responding to a mutational loss of Chi b, the organization of the photosystems for efficient light-utilization of photosynthesis. The present work was supported in part by Grant-in-Aid from the Ministry of Agriculture, Forestry and Fisheries (Integrated Research Program for the Use of Biotechnological Procedures for Plant Breeding II-3-2)-(l)-l. We thank Mrs. Shizue Sudo for her excellent technical assistance. References Arnon, D.I. (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24: Ghirardi, M.L., McCauley, S.W. and Melis, A. (1986) Photochemical apparatus organization in the thylakoid membrane of Hordeum vulgare wild type and chlorophyll Hess chlorina f2 mutant. Biochim. Biophys. Ada 851: Graan, T. and Ort, D.R. (1986) Detection of oxygen-evolving photosystem II centers inactive in plastoquinone reduction. Biochim. Biophys. Ada 852: Hsu, B.-D. and Lee, J.-Y. (1995) The photosystem II heterogeneity of chlorophyll ^-deficient mutants of rice: a fluorescence induction study. Aust. J. Plant Physiol. 22: Izawa, S., Kraayenhof, R., Ruuge, E.K. and Devault, D. (1973) The site of KCN inhibition in the photosynthetic electron transport pathway. Biochim. Biophys. Ada 314: Melis, A. (1982) Kinetic analysis of P-700 photoconversion: effect of secondary electron donation and plastocyanin inhibition. Arch. Biochem. Biophys. 217: Melis, A. (1985) Functional properties of photosystem II in spinach chloroplasts. Biochim. Biophys. Ada 808: Melis, A. (1990) Regulation of photosystem stoichiometry in oxygenic photosynthesis. In Regulation of Photosynthetic Processes. Bat. Mag. Tokyo, Special Issue 2. Edited by Miyachi, S., Kanai, R. and Katoh, S. pp Bot. Soc. Japan. Melis, A. (1991) Dynamics of photosynthetic membrane composition and function. Biochim. Biophys. Ada 1058: Melis, A. and Homann, P.H. (1975) Kinetic analysis of the fluorescence induction in 3-(3,4-dichlorophenyl)-l,l-dimethylurea poisoned chloroplasts. Photochem. Photobiol. 21: Murata, N. (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim. Biophys. Ada 172: Myers, J. (1971) Enhancement studies in photosynthesis. Annu. Rev. Plant Physiol. 22: Shen, J.-R., Satoh, K. and Katoh, S. (1988) Isolation of an oxygen-evolving Photosystem II preparation containing only one tightly bound calcium atom from a chlorophyll ^-deficient mutant of rice. Biochim. Biophs. Ada 936: Terao, T. and Katoh, S. (1989) Synthesis and breakdown of the apoproteins of light-harvesting chlorophyll a/b proteins in chlorophyll 6-deficient mutants of rice. Plant Cell Physiol. 30: Terao, T., Matsuoka, M. and Katoh, S. (1988) Immunological quantification of proteins related to light-harvesting chlorophyll a/b protein complexes of the two photosystems in rice mutants totally and partially deficient in chlorophyll b. Plant Cell Physiol. 29: Terao, T., Sonoike, K., Yamazaki, J., Kamimura, Y. and Katoh, S. (1996) Stoichiometry of photosystem I and II in rice mutants differently deficient in chlorophyll b. Plant Cell Physiol. 37: Terao, T., Yamashita, A. and Katoh, S. (1985a) Chlorophyll 6-defkient mutants of rice. I. Absorption and fluorescence spectra and chlorophyll a/b ratios. Plant Cell Physiol. 26: Terao, T., Yamashita, A. and Katoh, S. (1985b) Chlorophyll ^-deficient mutants of rice. II. Antenna chlorophyll o/6-proteins of photosystem I and II. Plant Cell Physiol. 26: (Received July 29, 1994; Accepted February 7, 1996)

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