lipid and fatty acid composition of chloroplast thylakoids isolated from betula pendula leaves in...

Lipid and Fatty Acid Composition of Chloroplast Thylakoids Isolated from Betula pendula Leaves in Different Stages of Development or Acclimated to Different Quantum Flux Densities

GUNNAR OQUIST1) and CONNY LILJENBERG2)

I) Department of Plant Physiology, University of Umea., S-901 87 Umea, Sweden and 2) Department of Plant Physiology, University of G6teborg, Carl Skottbergs Gata 22, S-413 19 G6teborg, Sweden

Received June 19, 1981 . Accepted July 10, 1981

Summary

The relative amounts and the fatty acid compositions of monogalactosyl diglyceride, digalactosyl diglyceride, sulpholipid and phospholipids of chloroplast thylakoids isolated from Betula pendula leaves in three different stages of development or acclimated to three different quantum flux densities were analyzed. Concomitant changes in the amount and properties of the acyl lipids and the size of the plastoquinone pool (and the light saturated rates of net photosynthesis and electron transport from water to nicotinamide adenine dinucleotide phosphate) were looked for. Data on plastoquinone and function are presented elsewhere (Oquist et aI., 1981 a, b). The comparisons were made in order to evaluate the feasibility of the hypothesis that the distribution or properties of acyl lipids regulate the electron transport rate by affecting the function of plastoquinone that is thought to be positioned in the hydrophobic core of the lipid double layer. The high rates of light saturated electron transport or net photosynthesis obtained during the course of leaf development, were paralleled by (1) a high ratio of galactolipidsl phospholipids, by (2) an increase in the level of unsaturation of first of all the galactolipids and by (3) a high content of trans-3-hexadecanoic acid in the phospholipid fraction. Chloroplast thylakoids isolated from birch seedlings acclimated to the contrasting light regimes showed, despite pronounced differences in photosynthesis function, only minor differences in the relative amounts and properties of the acyl lipids. However, high rates of photosynthesis in the high light acclimated seedlings were paralleled by a high content of trans-3-hexadecanoic acid. The differences in the relation between function and distribution or properties of acyl lipids seen between developing and differently light acclimated leaves are thought to depend on differences in experimental design; i.e. changes during ontogeny of leaves vs. the use of primarily mature leaves fully acclimated to a certain light regime. At present, we believe that the functional properties of plastoquinone, at least during the course of activity changes, is somehow

Abbreviations: DCMU, 3-(3,4-dichlorophenyl)-1,1-dimethylurea; DGDG, digalactosyl diglyceride; HEPES, N-2-hydroxyethyl-piperazine-N-2-ethane-sulphonic acid; MGDG, monogalactosyl diglyceride; NADP, nicotinamide adenine dinucleotide phosphate; PL, phospholipids; PQ, plastoquinone; Q, primary electron acceptor of photosystem II; SL, sulpholipid.

Z. Pjlanzenphysiol. Ed. 104. s. 233-242. 1981.

234 GUNNAR OQUIST and CONNY LILJENBERG

related to factors such as the ratio galactolipids/phospholipids, the unsaturation level of galactolipids and/or the content of trans-3-hexadecanoic acid. Whether this means that the properties of the acyl lipids are directly or only indirectly related to the function of plastoquinone can at present not be concluded.

Key words: Betula pendula, acyl lipids, chloroplast thylakoids, development.

Introduction

Studies of adaptation/acclimation in photosynthesis in response to contrasting environmental conditions have revealed responses at different levels of plant organization (Bjorkman, 1973; Boardman, 1977). In the chloroplast thylakoid membranes, the electron transport component plastoquinone A-45 seems to have a key function in regulating the rate of light saturated electron transport. One form of PQ, possibly a semiquinone, acts as the primary electron acceptor of PS-II, whereas the bulk pool of PQ links a vectorial electron and proton flow from PS-II and the outside of the thylakoid to the «Rieske»-ironsulphur protein on the inside of the thylakoid (Amesz, 1977; Trebst, 1978; White et aI., 1978; Witt, 1979). The size of this PQ pool, which is common to several photosynthetic units is, like the potential electron transport rate, smaller in shaded than in exposed plants (Bjorkman, 1973; Oquist et aI., 1981 a). Frost hardened pine seedlings with a lower light saturated electron transport rate than a control show a similarly reduced pool size of functional PQ (Oquist and Hellgren, 1976), and winter inhibition of pine photosynthesis occurs at the PQ level (Oquist and Martin, 1980). In addition, the electron transport between the two photosystems in chloroplasts isolated from developing leaves seems to be restricted at the site of PQ (Sestak, 1977; Oquist et aI., 1981 b). Senger and Fleischhacker (1978) have ascribed the different light saturated electron transport rates of Scenedesmus grown in low and in high quantum flux densities to different reoxidation rates of reduced PQ. This suggestion is consistent with the fact that the overall electron transport is rate limited at the site where PQ is reoxidized (Witt, 1979).

PQ is the most lipophilic major component of the electron transport chain and it can easily be extracted from freeze-dried thylakoids by non-polar solvents (Bishop, 1959). The picture currently emerging is that PQ function as interface molecules which, possibly by diffusion in the lipophilic matrix of the thylakoid, interconnect the reduced site of the PS-II reaction center protein (PQH2 is formed) with the site for PQH2 oxidation on the «Rieske»-ironsulphur protein.

The lipophilic association of PQ, as well as the limitation and regulation of the electron transport rate at the site of PQ, made us ask if environmentally induced changes in the bulk membrane acyl lipids and their fatty acids have a regulatory function on such properties as the functional pool size, the diffusion rate, or the reduction/ oxidation rate of PQ. We show elsewhere (Oquist, 1981) that winter inhibition of the electron transport of Pinus silvestris at the site of PQ occurs simultaneously with a relative decrease in the amount of MGDG (and of the MGDG + DGDG/PL

Z. Pjlanzenphysiol. Bd. 104. S. 233-242. 1981.

Thylakoid lipids of birch 235

and MGDG/DGDG ratios) and that the remaining MGDG fraction has an increased level of saturation. In naturally grown pine the correlation between the rate of overall electron transport from water to NADP and the unsaturation/saturation ratio of MGDG was very good (r = 0.93) when data obtained over one year were plotted together. Furthermore, MGDGI8 : 3 and PQ showed no interaction but a free miscibility in surface-balance technique studies (Liljenberg et al., 1980; Liljenberg, 1980), which probably means that PQ moves easily in a polyunsaturated bilayer of galactolipids. If 18: 3 of MGDG was saturated, however, PQ was squeezed out from the lipid layer. There is a possibility that the partial increase in saturation of MGDG in pine (Oquist, 1981) reduces the mobility of PQ so that its efficiency as an interface molecule decreases, thereby inhibiting the electron transport at the PQ-site.

As a contribution to our knowledge of the relationship between the PQ-activity and the lipids (fatty acids) we show in this study how leaf development and light acclimation affect the lipid and fatty acid composition of the chloroplast thylakoids of Betula pendula. The findings are discussed in relation to the sizes of the functional PQ pools (as determined by fluorescence kinetics) and the rates of electron transport of photosynthesis, as presented elsewhere (Oquist et al., 1981 a, b).

Materials and Methods

Seedlings of Betula pendula Roth. (B. verrucosa Ehrh.) were raised from seeds in climate chambers on aerated nutrient solutions (Anderson et al., 1977) at quantum flux densities of 50 (LL = low light), 250 (IL = intermediate light) and 600 (HL = high light) J,tmol quanta m-2s- 1

•

Temperatures were 25 and 15°C in light and dark, respectively. For full details see Brunes et al. (1980) and Oquist et aL (1981 a). All leaves from the plants were sampled together when assess· ing light acclimation effects on thylakoid lipids and fatty acids.

Lipid and fatty acid changes during leaf development were studied only in IL-plants. The following leaf populations were studied (per cent of total leaf area of the shoot is shown together with standard deviations for n = 10): leaves I, young and developing leaves at the top, 19.6 ± 4.7 %; leaves II, fully expanded and mature leaves taken from the middle of the plant, 55.7 ± 7.7 %; leaves III, old, shaded leaves of the lowest insertion, 28.8 ± 6.0 %. For more details see Oquist et aL (1981 b).

Chloroplasts were isolated as described elsewhere (Oquist et al., 1981 a). In order to rupture the chloroplasts, they were suspended in 0.05 M HEPES buffer pH 7.6 and the suspension was forced once through a French pressure cell at 1400 kg cm-2

• Intact chloroplasts were centrifuged down at 1,000 g for 10 min and the thylakoid membranes in the supernatant were harvested after centrifugation at 27,000 g for 30 min. All steps were performed at +4 0c.

The total lipid content of the thylakoids was first extracted with 20 ml ice-cold chloroform: methanol (2: 1, v/v) and the extracted thylakoids centrifuged down at 27,000 g for 5 min. The extraction of the pellet was then repeated with 20 ml chloroform : methanol (1 : 1, v/v) and finally with 20 ml chloroform: methanol (1 : 2, v/v) to which was added 6 ml 0.73 % NaCl in order to extract the most polar lipids. The supernatants after each extraction were combined and evaporated to dryness at 40°C. The residue was dissolved in chloroform and applied to a silicic acid column (Silicar CC7, Mallinckrodt). Lipids with increasing polarity were eluted with 1) chloroform (neutral lipids), 2) chloroform: acetone (1 : 1) followed by pure acetone (galactolipids + sulpholipid), and 3) methanol (phospholipids). Fractions 2) and 3) were taken to dryness and the lipids were separated by TLC (Silica Gel H, Merck) developed in



chloroform: methanol: acetic acid: H 20 (85: 15 : 10 : 3.6). The plates were dried in N2 atmosphere. The lipids were located by 12 vapour and bands with MGDG, DGDG, SL and PL (total) were scraped off and the lipids eluted with chloroform: methanol (2 : 1, v/v). For details see Nichols et aI. (1965), Rouser et al. (1967) and Sellden and Selstam (1976). The fatty acids of the lipids were converted to methyl esters using Sigma's 14 % boron trifluoride in methanol (Morrison and Smith, 1964). The methyl esters were then separated and identified by GLC (Perkin-Elmer 900) equipped with a 3.5 mm x 2 m glass column packed with 4.5 % butane-l,4-diol succinate (HI-EFF 4BP; Applied Sciences Lab. Inc.) on Chromosorb W A W-DMCS 80/100 (Applied Sciences Lab. Inc.). The column temperature was 180°C. Heptadecanoid acid (17 : 0) was used as standard.

Results

Leaves in different stages 0/ development

Chloroplast thylakoids of young, developing leaves I had significantly lower relative contents of MGDG, DGDG and SL than had the mature leaf populations II and III which did not differ in their relative lipid composition (Table 1). The combined

Table 1: Relative mol % of lipids in chloroplast thylakoids isolated from leaves (at three different stages of development) of Betula pendula grown at 250 ftmol quanta m-2

S-1

, and from integrated leaf samples from birch grown at three different quantum flux densities (50 = LL, 250 = IL and 600 = HL ftmol quanta m-2s-1

). The three leaf populations were: I, young, expanding leaves at the top; II, fully expanded, mature leaves of middle insertion; III, old, shaded leaves of lowest insertion. tr = trace and represent amounts less than 3 %. Standard deviations for indicated numbers of experiments are given.

MGDG DGDG SL PL MGDG! MGDG+ DGDG DGDG!

PL

19.8±3.8 16.0 ± 4.2 3.1 ±2.4 68.2 ± 13.5 1.2 0.5 n=4 (n=2)

II 37.3 ± 1.5 28.1±0.4 7.7±0.9 26.9± 1.5 1.3 2.4 n=3 III 32.7 ± 4.3 24.6±3.2 7.4 ± 1.3 35.2± 6.4 1.3 1.6 n=3

LL 37.1 ±4.8 19.6±1.6 5.9 ± 1.0 37.5± 7.2 1.9 1.5 n=3 IL 28.2 ± 1.8 29.0±5.2 8.6± 1.0 34.5± 5.5 1.0 1.7 n=3 HL 27.1 ±4.2 28.2 ± 1.2 7.1±1.4 37.6± 4.2 1.0 1.5 n=3

amount of the phospholipids, PL, was high and was the dominating lipid group in the chloroplast thylakoids of leaves I. In thylakoids isolated from leaves II and III, however, the two galactolipids dominated. A common property of all lipids was that the ratio of unsaturated/saturated fatty acids increased with leaf maturation, especially for MGDG, DGDG and SL (Tables 2 and 3). The fatty acid data of SL in leaves I must be treated with caution because the results were, for reasons we do not understand, quite variable (Table 2). The increases of the unsaturation/saturation ratios were mainly achieved by decreasing the proportion of palmetic acid (16 : 0) and



Table 2: Relative mol % of fatty acids of lipids isolated from chloroplast thylakoids of Betula pendula leaves at three different stages of development and of integrated leaf samples taken from birch grown at three different quantum flux densities. For details see Table 1. 16 : 0, palmitic acid; 16: 1,trans-3-hexadecanoicacid;18: 0, stearic acid; 18 : 1, oleic acid; 18 : 2, linoleic acid; 18 : 3, linolenic acid.

II III

16 : 0 16 : 1

M 20.5 ± 4.7 tr

404 ± 0.5 tr 5.6 ± 1.7 tr

16 : 3

G o tr tr

18 : 0 18 : 1 18 : 2 18 : 3

D G 5.1 ±0.7 8.6±4.0 504± 1.4 56.9± 12.7 n=3 tr tr 5.0±004 89.3± 1.0 n=3 tr tr

LL 3.7 ± 0.3 tr 3.1 ± 0.1 tr tr tr tr

404±0.3 86.5± 1.2 n=4

3.8± 1.9 8904± 1.7 n=3 6.9±0.9 87.4± 2.1 n=3 6.8±2.2 83.7± 7.1 n=3

IL 4.8 ± 1.0 tr HL 604 ± 2.0 tr

D 36.7± 2.8 tr

II 23.6± 1.9 0 III 2604± 1.8 tr

LL 22.5± 2.1 tr

IL 28.5± 5.1 0 HL 27.5 ± 0.9 0

87.7 ± 21.3 0 II 51.0± 3.0 0 III 59.8± 1.9 0

LL 46.9± 1.5 tr IL 53.2 ± 2.7 0 HL 57.2 ± 4.0 0

tr o G o o o tr o o S o o o tr o o

II III

P 31.9± 1.7 tr 0 22.6± 0.9 1304±1.7 0

LL IL HL

28.0 ± 2.0 9.2 ± 2.9 tr

28.1± 3.7 504±0.1 tr 23.6± 0.2 14.6± 1.0 0 27.0 ± 2.7 13.9 ± 2.9 0

tr tr

D G 4.5 ± 0.3 tr 5.6±4.6 51.7± 0.1 n=2 tr tr 3.1±0.3 72.3± 2.8 n=3 tr tr 5.0±0.2 68.8± 1.1 n=4

2.1±0.1 tr 4.0±0.0 68.2± 2.7 n=3 tr tr 4.5±0.3 64.1± 7.5 n=3 tr tr 304±0.2 66.3± 204 n=3

L 4.8±3.1 6.2±5.5 tr 7.3± 7.5 n=3 tr 3.3 ± 0.2 5.3 ± 0.7 40.3 ± 204 n = 3 tr tr tr 36.5± 1.9 n=2

2.8±0.6 6.3±0.7 6.3±1.1 37.6± 0.9 n=3 tr 3.5±0.2 7.6±1.4 35.6± 2.5 n=3 tr 3.2±2.7 504±0o4 33.0± 5.3 n=3

L tr tr tr

tr tr tr

6.5±1.1 4.6±0.2 4.5 ± 0.2

6.7±0.6 7.0 ± 1.0 5.3 ± 0.3

31.6± 1.8 2804± 3.6 n=4 20.2 ± 0.5 39.2 ± 1.7 n = 3 12.7 ± 0.8 45.2 ± 2.5 n = 3

19.6±1.8 38.5± 4.1 n=3 23.3±004 30.7± 1.1 n=3 21.1 ±0.9 31.7± 2.6 n=3

Table 3: The ratio unsaturated/saturated (16 : 1 + 16 : 3 + 18 : 1 + 18 : 2 + 18 : 3/16 : 0 + 18 : 0) fatty acids of lipids isolated from chloroplast thylakoids of Betula pendula leaves at three different stages of development and of integrated leaf samples taken from birch grown at three different quantum flux densities. For details see Table 1.

II III

LL IL HL

MGDG

4.0 21.4 17.1

26.0 19.7 14.1

DGDG

0.6 3.2 2.7

2.9 204 2.5

SL

0.1 1.0 0.5

1.0 0.9 0.7

PL

2.2 304 2.7

2.5 3.2 2.7


increasing the proportion of linolenic acid (18 : 3) as leaves I developed into leaves II. It can, however, be noticed that only traces of 18 : 0 and 18 : 1 were found in thylakoids of leaves II and III, whereas these acids had a higher relative content in the thylakoids of leaves I. Another difference between developing leaves I and mature leaves II and III was seen in the fatty acid composition of PL. Only traces of trans-3-hexadecanoic acid (16: 1), which is only reported in phosphatidyl glycerol (GuillotSalomon et al., 1978), coule! be observed in PL isolated from thylakoids of leaves I whereas about 10 % of the fatty acids of PL consisted of 16 : 1 in the mature leaf chloroplasts. The fatty acid composition of leaves II and III did not differ significantly.

Acclimation to different quantum flux densities

Chloroplast thylakoids isolated from integrated leaf samples of birch seedlings acclimated to low and high quantum flux densities showed no major differences in the relative proportions of the bulk acyl lipids (Table 1). There was, however, a tendency for MGDG to decrease and DGDG to increase with increasing light. This resulted in the MGDG/DGDG ratio in chloroplast thylakoids of IL and HL plants being half that of LL plants. Nor could any major changes induced by the light level be detected in the composition of fatty acids in the individual lipids (Table 2) although there might be a tendency for-MGDG to become more saturated with increased quantum flux density (Table 3). The content of 16: 1 in PL was significantly lower in LL-plants than in IL- and HL-plants (Table 2).

Discussion

The pronounced relative increases of both MGDG and DGDG, as a consequence of leaf maturation (Table 1), agree with previous reports showing a relative increase in the content of galactolipids in chloroplast thylakoids during chloroplast and tissue development (Roughan and Boardman, 1972; Leese and Leech, 1976). However, we cannot exclude the possibility that the differences in the MGDG + DGDG/PL ratios are also influenced by thylakoid preparations of developing and mature leaves containing different proportions of plastide membranes other than thylakoids. The ratios of unsaturated/saturated fatty acids of the individual lipids increased as a consequence of leaf maturation (Table 3). This is consistent with an increasing desaturation activity found during chloroplast development (Tnfmolieres and Lepage, 1971; Mackender, 1979) although there are also reports that the relative distribution of fatty acids does not change during chloroplast development (Roughan and Boardman, 1972; Sellden and Selstam, 1976).

The increase of trans-3-hexadecanoic acid (16 : 1) in PL (or more accurately in phosphatidyl glycerol) when birch leaves mature (Table 2) agree with many previous reports showing an appearance of 16: 1 during greening (Roughan and Boardman, 1972). The synthesis of 16 : 1 has been correlated with the onset of DCMU sensitive

Z. Pjlanzenphysiol. Bd. 104. s. 233-242. 1981.


electron transport (Sellden and Selstam, 1976) and with grana formation (GuillotSalomon et aI., 1978).

The pronounced increases of the ratio MGDG + DGDG/PL (Table 1) and of the unsaturation/saturation ratios of MGDG and DGDG (Table 3) induced during development, were paralleled by an eight-fold increase of the PQ/Q ratio and twoand four-fold increases of the light-saturated rates of net photosynthesis and electron transport from water to NADP, respectively (d. Oquist et aI., 1981 b). Similar parallel changes of the acyl lipids and of the function of the thylakoids have been observed in naturally grown Pinus silvestris during the course of one year (Oquist, 1981). When the photosynthetic electron transport during autumn and early winter gradually became inhibited at the site of PQ, there were concomitant decreases of the unsaturation/saturation ratio of MGDG (but not of DGDG) and of the ratios of MGDG + DGDG/PL and MGDG/DGDG. Reverse changes occurred during spring and early summer. There was a very good correlation (r = 0.93) between the light saturated rates of electron transport over PQ and the unsaturationl saturation ratios of MGDG if the pine data of one year were combined in a linear regression plot. Since we have shown elsewhere (Liljenberg et al., 1980; Liljenberg, 1980) that the free molecular miscibility between MGDG and PQ decreases when linolenic acid (18 : 3) becomes saturated, we may suggest that the activity of the lipophilic electron transport carrier PQ in developing birch leaves, as well as in pine exposed to natur~l climatic variations (Oquist, 1981), is influenced by the saturation level of the galactolipids.

The idea that there is a functional interaction between the electron transport and lipids of the thylakoids is supported by the finding of Heise and Harnischfeger (1978) that the P/2e ratio in spinach chloroplast thylakoids increases with the MGDG/PL ratio. The idea that there is a relationship between the level of saturation of the galactolipids and the function of PQ is, however, opposed by recent results of Restall et ai. (1979). They report that hydrogenation of spinach chloroplast lipids to about 40 % did not have any marked effects on the rate of electron transport from water to

methyl viologen. Furthermore, the hypothesis of a functional interaction between PQ and the mentioned properties of the acyl lipids receives little support from the results of the light acclimation study of birch (Tables 1-3). When the size of the functioning PQ pool and the rates of net photosynthesis and electron transport from water to NADP increased two to three times (Oquist et aI., 1981 a), as a result of acclimation to higher quantum flux densities, there was a two-fold decrease of the MGDG/DGDG ratio [this ratio did not vary between leaves in different stages of development and it changed in comparison with the electron transport in the opposite direction in pine (Oquist, 1981)], a tendency to an increase of the saturation level of MGDG (opposite to what was found for developing birch leaves and for pine), and a two-fold increase of trans-3-hexadecanoic acid (16: 1) (the same was found for developing birch leaves and for pine).

The reason why developing birch leaves and naturally grown pine showed similar

z. Pjlanzenphysiol. Ed. 104. s. 233-242. 1981.


and parallel changes in their acyl lipids and rates of electron transport, differing (except in the case of 16 : 1) from those observed when birch was acclimated to different light regimes, is thought to depend on differences in experimental design. In developing birch leaves and pine, changes in electron transport and lipids were studied as a function of time, i.e. ontogeny and climatic changes over a year, whereas in the light acclimation study the birch seedlings were adapted to constant climatic environments, where, irrespective of light regime, they showed equal photosynthetic quantum yields under light limiting conditions (Oquist et aI., 1981 a).

In conclusion the results of this work (and results reported elsewhere [Oquist, 1981] for naturally grown pine) show that there during the course of changes in the activity of PQ parallel changes occur in the level of saturation of the galactolipids and in the ratio between galactolipids and phospholipids. Whether this means that the properties of the acyl lipids have a direct regulatory function on the activity of PQ (at least during the course of activity changes), or that the observed parallel changes in the two parameters are only indirectly related, can at present not be concluded. For this purpose more correlative research is necessary as well as model experiments with monolayer films (where PQ is mixed with different ratios of acyl lipids and with galactolipids showing different unsaturationl saturation ratios) or with artificial bilayer membranes. Special attention should be paid to the finding that high electron transport rates over PQ in all studied cases were paralleled by high contents of trans-3-hexadecanoic acid (16: 1) in PL. Is it possible that this acid affects the boundary layer molecular properties of PL and therefore also the functional sites where reduced PQ is oxidized?

Acknowledgement

The skilful technical assistance of Monica Hallen is gratefully acknowledged. This investigation was supported by the Swedish Natural Science Research Council.

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