Variable stoichiometries of photosystem II to photosystem I reaction

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Variable stoichiometries of photosystem II to photosystem I reaction centres. Prior to 1980 it was assumed that in the grana of plant chloroplasts the two.

Photosynthesis Research 17:277-281 (1988) © Kluwer AcademicPublishers, Dordrecht - Printed in the Netherlands Letter to the Editor*

Variable stoichiometries of photosystem II to photosystem I reaction centres Prior to 1980 it was assumed that in the grana of plant chloroplasts the two photosystems (PS) were organized as a supercomplex. Then Andersson and Anderson (1980) proposed that PSI was totally excluded from the appressed membranes of the grana stacks, where most PS II complexes and their associated chlorophyll (Chl) a/b-proteins (LHC II) were located. Final proof for an extreme lateral heterogeneity in the distribution of P S I now comes from immunocytochemical studies which directly demonstrate that P S I is present only in non-appressed membranes (Vallon et al. 1986, Anderson and Goodchild 1987). Given that P S I and PS II complexes are structurally and functionally autonomous and that PS I is involved in both cyclic and non-cyclic electron transport, there is no need for equal or fixed numbers of P S I and PS II complexes (Anderson 1981, Anderson 1982), which were first assumed in the Z scheme and subsequently advocated by Whitmarsh and Ort (1984). Indeed, Melis and Brown (1980) first reported variable PS II/PS I reaction centre ratios in plant thylakoids. As summarized below, our research consistently shows variable stoichiometries of PS II/PS I reaction centres for plants grown either under controlled light conditions (1, 2 below) or in natural habitats (3, 4 below). (1) Growth irradiance: With increasing irradiance for growth, there is a marked increase in the amount of P680 per total chlorophyll; in contrast, the PT00/Chl ratios are unaltered. Hence there is an increase in the PS II/PS I reaction centre ratio with acclimation to increasing growth irradiance as shown in Table 1 (Leong and Anderson 1984, Chow and Hope 1987, Evans 1987, Chow et al. 1988, see also Wild et al. 1986). (2) Adaptation to altered irradiance: Following the transfer to high irradiance of pea plants fully adapted to low irradiance, marked modulations occur in the composition and function of their thylakoid membranes (Chow and Anderson 1987a, 1987b). The ratio of the PS II to PSI reaction centres increased from 1.25 to 1.7 within 6 days after transfer from low to high irradiance. (3) Shade-tolerant species: Shade-tolerant plants have lower PS II/PS I reaction centre ratios closer to unity when grown under shade or low light, * This is the first letter on the topic of the ratio of Photosystems I and II. Additionalletters on this topic are welcomed. - R. Blankenship, Editor.

278 as shown in Table 1 (Anderson et al. 1988). These ratios are lower than those found in sun-species, whether PS II is determined via the O2-yield per single-turnover flash with leaf discs (Table 1) or from the number of DCMU- or atrazine-binding sites (not shown). Consistent with this, shade plants with lower Chl a/Chl b ratios have more LHC II, and concomitantly less core Chl a-proteins of PS II (Anderson 1986). In contrast, Melis and Harvey (1981) found higher PS II/PS I ratios for shade than sun plants, using as an assay for PS II the light-induced absorbance change at 320 nm, for which appropriate correction for flattening would be necessary. (4) Chl b-less barley mutant: The Chl b-deficient barley mutant with no LHC II or LHC I has a higher PS II/PS I reaction centre ratio than the wild-type barley (Table 1), in agreement withe the results of Ghirardi et al. (1986). We conclude that sun/shade acclimation or adaptation to irradiance combines two strategies: adjustments in both the PS II/PS I reaction centre ratios and the antenna size of PS II, Relative to PS I, shade plants have fewer, though larger PS II units to maximise light-harvesting (Anderson et al. 1988). Sun plants have more, though smaller PS H units relative to P S I units; a smaller antenna of PS II in plants grown in full sunlight should confer greater resistance to photoinhibition. It is possible that variations in the P680/P700 ratios from different laboratories or plants result from varying degrees of inactivation of functional PS II centres during thylakoid isolation. To overcome this difficulty, we have Table 1. PS I I / P S I reaction centre r a t i o s in different species g r o w n in h i g h or l o w light.

spinach pea

Alocasia macrorrhiza lettuce Chl b-less barley wild-type barley

Dianella revoluta Colysis ampla Helmholtzia glabberima

H i g h light

L o w light

2.21Y' 2.29 ~ 2.09 b 2.02 a 3.13 a 2.14 a -

1.14 c 1.25 c 1.43 d 1.21 c 1~43e 1.26 f


1.63 a

P S 1 centres were determined by light-induced absorption changes at 703 nm in thylakoid suspensions after subtracting the chlorophyll fluorescence artifact. Functional P S H centres were determined directly in leaf discs~segments from the 02 evolution per single turnover flash in the presence of background far-red light (&radiance I "~ 171zmol photons m-2 s -I, 700-730nm). a. Full glasshouse light (I ~- 1000 at mid-day), b. Fluorescent light, I ~- 700. c. Fluorescent light, I ~- 80. d. Incandescent light, I " 10. e. Underneath tree canopy, I "~ lO.f. Shadedglasshouse light I " 10. The units for irradiance (I) are Fmol photons m-2 s -1. Data are from Fig. 2 in Anderson et al. (1988), except for Chl b-less barley which in the present table was grown in glasshouse sunlight, while in Anderson et al. (1988) was grown under fluorescent light. Species in italics are shade-tolerant.

279 developed a method to determine the functional PS II centres in leaves using background far-red light to keep the plastoquinone pool oxidised (Chow et al. 1988). There is a linear relationship between the number of functional PS II reaction centres in leaves, and the DCMU-binding sites of their isolated thylakoids. Significantly, there is only 15% difference between the two sets of measurements, DCMU-binding sites being more abundant. The difference is in any case partly attributable to a miss factor in the flash-induced 02 evolution (Chow and Hope 1987) and to the fact that the flash intensity is just less than saturating for leaf discs. We find no evidence for large pools of non-functional PS II units as advocated by Graan and Ort (1986) for isolated thylakoids. Indeed, to our knowledge, a large pool of non-functional PS II units has not been demonstrated in vivo in non-stressed leaves. In conclusion, our results (regardless of the method used to assay PS II) consistently demonstrate that there are no fixed, invariant stoichiometries of PS II to P S I reaction centres, contrary to the proposal by Whitmarsh and Ort (1984). Further we do not favour the suggestion of a large pool of non-functional PS II units in intact chloroplasts (Graan and Oft 1986). Instead, plant thylakoids with membrane stacking permit an extreme lateral heterogeneity in the distribution of the photosystems, and hence no fixed stoichiometries between them are needed. Acclimation to light involves complex regulation at the level of synthesis, assembly and degradation of thylakoid complexes. Two strategies are combined: there are both adjustments to the PS II/PS I reaction centre ratio, as well as to the light-harvesting antennae. These changes occur in leaves throughout the canopy, and also across leaves themselves (Terashima and Takenaka 1986). The membrane architecture of thylakoids is dynamic: short-term regulatory mechanisms, as yet barely characterized, also allow rapid, reversible structural re-organization of existing complexes, particularly of the peripheral pool of LHC II, to cope with sudden environmental changes (Anderson and Andersson 1988). ~CSIRO, Division of Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia; 2School of Biological Sciences, Flinders University, Bedford Park, SA 5042 Australia Received 19 February 1988; accepted 29 March 1988

W.S. Chow ~ Jan M. Anderson t A.B. Hope 2

280 References Anderson JM (1981) Consequences of spatial separation of photosystem 1 and 2 in thylakoid membranes of higher plant chloroplasts. FEBS Lett 124:1-10 Anderson JM (1982) The role of chlorophyll-protein complexes in the function and structure of chloroplast thylakoids. Mol Cell Biochem 46:161-172 Anderson JM (1986) Photoregulation of the compostion, function and structure of thylakoid membranes. Ann Rev Plant Physiol 37:93-136 Anderson JM and Andersson B (1988) The dynamic photosynthetic membrane and regulation of solar energy conversion. Trends Biochem Sci, 13: in press Anderson JM and Goodchild DJ (1987) Lateral distribution of the photosystem I complex between the appressed and non-appressed regions of spinach thylakoid membranes: an immunocytochemical study. In: Biggins J (ed.) Progress in Photosynthesis Research, Vol. 2, pp. 301-304. Dordrecht: Martinus Nijhoff Anderson JM, Chow WS and Goodchild DJ (1988) Thylakoid membrane organization in sun/shade acclimation. Aust J Plant Physiol 15:11-25 Andersson B and Anderson JM (1980) Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim Biophys Acta 593:427-440 Chow WS and Anderson JM (1987a) Photosynthetic responses of Pisum sativum to an increase in irradiance during growth. I. Photosynthetic activities. Aust J Plant Physiol 14:1-8 Chow WS and Anderson JM (1987b) Photosynthetic responses of Pisum sativum to an increase in irradiance during growth. II. Thylakoid membrane components. Aust J Plant Physiol 14:9-19 Chow WS and Hope AB (1987) The stoichiometries of supramolecular complexes in thylakoid membranes from spinach chloroplasts. Aust J Plant Physiol 14:21-28 Chow WS, Hope AB and Anderson JM (1988) Oxygen per flash from leaf disks quantifies Photosystyem II. Submitted to Biochim Biophys Acta Evans JR (1987) The relationship between electron transport components and photosynthetic capacity in pea leaves grown at different irradiances. Aust J Plant Physiol 14:157-170 Ghirardi ML, McCauley SW and Melis A (1986) Photochemical apparatus organization in the thylakoid membrane of Hordeum vulgate wild type and chlorophyll b-less chlorina t"2 mutant. Biochim Biophys Acta 851:331-339 Graan T and Ort DR (1986) Detection of oxygen-evolving Photosystem II centers inactive in plastoquinone reduction. Biochim Biophys Acta 852:320-330 Leong TY and Anderson JM (1984) Adaptation of the thylakoid membranes of pea chloroplasts to light intensities. II. Regulation of electron transport capacities, electron carriers, coupling factor (CF~) activity and rates of photosynthesis. Photosynth Res 5:117-128 Melis A (1984) Light regulation of photosynthetic membrane structure, organization and function. J Cell Biochem 24:271-285 Melis A and Brown JS (1980) Stoichiometry of system I and system II reaction centers and of plastoquinone in different photosynthetic membranes. Proc Natl Acad Sci USA 77: 4712~1t716 Melis A and Harvey GW (1981) Regulation of photosystem stoichiometry, chlorophyll a and chlorophyll b content and relation to chloroplast uitrastructure. Biochim Biophys Acta 637: 138-145 Terashima I and Takenaka A (1986) Organization of photosynthetic system of dorsiventral leaves as adapted to the irradiation from the adaxial side. In: Marcelle R, Clijsters H and Van Poucke M (eds) Biological Control of Photosynthesis, pp. 219-230. Dordrecht: Martinus Nijhoff

281 Vallon O, Wollman FA and Olive J (1986) Lateral distribution of the main protein complexes of the photosynthetic apparatus in Chlamydomonas reinhardtiiand in spinach: an immunocytochemical study using intact thylakoid membranes and a PS II enriched membrane preparation. Photobiochem Photobiophys 12:203-220 Whitmarsh J and Ort DR (1984) Stoichiometries of electron transport complexes in spinach chloroplasts. Arch Biochem Biophys 231:378-389 Wild A, H6pfner M, Riihle W and Richter M (1986) Changes in the stoichiometry of photosystem II components as an adaptive response to high-light and low-light conditions during growth. Z. Naturforsch 41c: 597-603

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