Journal of Experimental Botany, Vol. 52, No. 365, pp. 2275-2282,
December 1, 2001
© 2001 Oxford University Press
Original Papers |
Age-dependent variation in membrane lipid synthesis in leaves of garden pea (Pisum sativum L.)
Department of Plant Physiology, Botanical Institute, Göteborg University, PO Box 461, SE-405 30 Göteborg, Sweden
Received 1 March 2001; Accepted 5 July 2001
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Abstract |
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To study membrane lipid synthesis during the life-span of a dicotyledon leaf, the second oldest leaf of 10–40-d-old plants of garden pea (Pisum sativum L.) was labelled with [1-14C]acetate and the distribution of radioactivity between the major membrane lipids was followed for 3 d. In the expanding second oldest leaf of 10-d-old plants, acetate was primarily allocated into phosphatidylcholine (PC) during the first 4 h of labelling. During the following 3 d, labelling of PC decreased and monogalactosyldiacylglycerol (MGDG) became the most radioactive lipid. In the fully expanded second oldest leaf of older plants, acetate was predominantly allocated into phosphatidylglycerol (PG), which remained the major radiolabelled lipid during the 3 d studied. The proportion of radioactivity recovered in MGDG decreased with increasing plant age up to 20 d, suggesting that, in expanded leaves, MGDG is more stable and requires renewal to a lower extent than PG. When the second oldest leaf approached senescence, labelling of MGDG again increased, indicating an increased need for thylakoid repair. The proportion of acetate allocated into phosphatidylethanolamine and free sterols was largest in leaves of 18–26-d-old plants and in the youngest leaves, respectively. Thus, these results demonstrate that the distribution of newly synthesized fatty acids between acyl lipid synthesis in the chloroplast and extraplastidial membranes strongly varies with leaf age, as do the proportion utilized for sterol synthesis. The findings emphasize the importance of defining the developmental stage of the leaf material used when performing studies on leaf lipid metabolism.
Key words: Galactolipid, lipid metabolism, monogalactosyldiacylglycerol, phosphatidylglycerol, Pisum.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Synthesis of leaf membrane lipids occurs as a co-operation between chloroplasts and the endoplasmic reticulum (Ohlrogge and Browse, 1995
). Fatty acid synthesis occurs predominantly in the chloroplasts. In all plants, newly synthesized fatty acids are utilized within the chloroplast for the synthesis of phosphatidylglycerol (PG), as well as exported to the cytosol during the formation of acyl-CoAs in the chloroplast envelope. The acyl-CoAs are primarily utilized in phospholipid synthesis in the endoplasmic reticulum, where synthesis of free sterols also occurs. The bulk of the phospholipids and sterols synthesized in the endoplasmic reticulum are exported to other membranes of the cell (Moreau et al., 1998). The endoplasmic reticulum also provides the chloroplasts with acylglycerol backbones for the synthesis of the bulk of the thylakoid lipids, monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), both of which are synthesized in the chloroplast envelope (Marechal et al., 1997). It has been suggested that the precursor diacylglycerol (DAG) derives from PC, formed in the chloroplast envelope by acylation of lyso-phosphatidylcholine (lysoPC), which has been transported from the endoplasmic reticulum to the chloroplast (Mongrand et al., 1997, 2000). Recently, this hypothesis was challenged by Williams et al., who suggested that DAG itself may be the lipid transported to the chloroplast (Williams et al., 2000). So-called 18:3 plants (e.g. Pisum) totally depend on this extra-plastidic lipid source, whereas so-called 16:3 plants (e.g. Arabidopsis, Spinacia) can produce a portion of its galactolipids entirely within the chloroplast (Ohlrogge and Browse, 1995; Moreau et al., 1998).
Although in situ leaf membrane lipid metabolism has been the object of numerous investigations, the focus usually has been on restricted time periods (Slack and Roughan, 1975; Mongrand et al., 1997, 2000; Williams et al., 1998a, b), on the effects caused by senescence (Wanner et al., 1991; Meir and Philosoph-Hadas, 1995), or on abiotic stress (Pham Thi et al., 1985; Hellgren et al., 1995; Carlsson et al., 1996). Thus a basic knowledge concerning the normally occurring variations in membrane lipid metabolism during the entire life span of a leaf is still lacking. The purpose of the present study was to determine the relative demands for newly synthesized fatty acids in plastidial and non-plastidial acyl lipid synthesis, respectively, during the life span of a leaf. Another aim was to determine whether any alterations occurred in the turnover of sterols versus non-plastidial phospholipids. To this end, the radiolabel associated with the membrane lipids of the second oldest leaf of 10–40-d-old garden pea plants, which had been administered with [1-14C]acetate was analysed. Garden pea was chosen for two reasons: it is an 18:3 plant, which means that chloroplast PG is the only lipid synthesized entirely within its chloroplasts, and as most studies on lipid metabolism in relation to leaf tissue age have been performed with monocotyledons, data are missing on the alterations in lipid metabolism that occur during natural ageing in leaves of dicotyledon species. However, it should be kept in mind that young leaves of dicotyledons are more heterogenous as to cell age, than sections of a monocotyledon leaf.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Materials
Seeds of garden pea (Pisum sativum L. cv. Kelvedon Wonder [Svalöv-Weibull, Landskrona, Sweden]) were soaked for 24 h in running tap-water at 25 °C and sown in fertilized soil. The plants were grown in a climate chamber as previously described (Carlsson et al., 1994
), except that the temperature was 23/18 °C and RH 70/80% during the light/dark periods, respectively. Five days after sowing, seedlings of similar size were transplanted in pairs into fertilized soil in plastic pots (13.5 cm wide, 11.5 cm high). Plants were irrigated with deionized water and fertilized from day 15 onward. Ten to 40-d-old pea plants were used (soaking of seeds started at day 0). All chemicals and organic solvents were of analytical grade. Salts, organic solvents and TLC plates were from Merck (Darmstadt, Germany), reference lipids and fine chemicals were from Sigma (St Louis, MO, USA) and the sodium[1-14C]acetate was from Amersham Pharmacia Biotech (Uppsala, Sweden).
Labelling with [14C]acetate
[1-14C]acetate was chosen as substrate as it is rapidly converted to acetyl-CoA, the major primer for fatty acid biosynthesis (Post-Beittenmiller et al., 1992).
Ten µl of a solution of sodium[1-14C]acetate in 0.02% (w/v) sodium deoxycholate was pipetted in situ onto the upper surface of one of the leaflets of the second oldest leaf of 10–40-d-old plants. Care was taken to ensure that the volume was distributed over the entire leaflet surface. The administered radioactivity per leaflet was 0.148 MBq, corresponding to 80 nmol sodium acetate. The detergent concentration used did not cause any visible lesions on the leaves, nor did it alter the distribution of radiolabel between the compounds investigated. In the presence of the detergent, radiolabel incorporation into extractable compounds increased substantially, reflecting that the detergent facilitated acetate uptake through the leaf surface (result not shown).
Lipid extraction and analysis
For each plant age, a radiolabelled leaflet was sampled 4, 24 and 72 h after radiolabelling. The leaflets were weighed, the surface wash rinsed with distilled H2O and immediately afterwards, lipids were extracted as previously described (Carlsson et al., 1994), except that the entire leaflet was used. Aliquots of the chloroform and aqueous phases from the lipid extraction were sampled for the determination of radioactivity by liquid scintillation counting, as described earlier (Hellgren et al., 1995). Lipids were separated by TLC and the distribution of radioactivity between the different lipid classes, were determined by TLC radioscanning as earlier described (Hellgren et al., 1995).
Data presentation
Lipid classes that throughout the experiment each retained less than 1% of the lipid radioactivity recovered has been omitted from the presentation (lyso-acyl lipids, phosphatidic acid, phosphatidylinositol, diphosphatidylglycerol, triacylglycerol, diacylglycerol, free fatty acids, sterol derivatives). The presented data are the average values from analyses of the second oldest leaf of at least four independently cultivated plants for each plant age and harvest time.
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Plant development
The second oldest leaf was still expanding in the youngest, 10-d-old pea plants. In 14-d-old plants, expansion of this leaf had ceased, as the fresh weight of the sampled leaflet did not increase further from plant age 14 d (Table 1
). Flowering began when the plants were 27–30-d-old, and seedpods started to develop in 29–32-d-old plants. The first visible signs of senescence of the sampled leaves were observed in 39–41-d-old plants as chlorotic spots at the leaf margins. In 40-d-old plants, about 50% of the leaves in the study had some chlorotic spots. At the last sampling occasion, when the plants were 43-d-old, three out of four harvested leaflets had chlorotic spots, and one out of four leaflets had also started to show signs of decreasing turgor.
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Distribution of radioactivity between lipids and non-lipid compounds
All leaves were administered with the same amount of radiolabel. Nevertheless, the total amount of radioactivity recovered in the lipid fraction varied between the independent experiments, probably due to differences between independently cultivated plants in acetate uptake or in the proportions of acetate allocated into non-extracted components or compounds exported to other parts of the plant. However, for each plant age, the distribution of radiolabel between the lipids did not appear to be affected by the proportion of the administered acetate that was allocated to the lipid fraction. However, the proportion of the administered radioactivity recovered in the lipid extract 3 d after radiolabelling decreased from around 60% in the still expanding leaves of the 10-d-old plants to 17–20% in the fully expanded leaves of older plants (results not shown).
In order to determine whether the capability to channel the added [1-14C]acetate to lipid synthesis varied with leaf age, the distribution of radioactivity between the chloroform and aqueous phases of the lipid extraction was analysed. Synthesis of lipids and lipid-soluble compounds was more active in the still expanding leaf of the 10-d-old plants than in the fully expanded leaf of older plants (Fig. 1A–C). In the 10-d-old plants, more than 90% of the recovered radiolabel was lipid associated 72 h after radiolabelling, whereas in the older plants, approximately 65–75% of the extractable radiolabel was lipid-associated 72 h after the administration of [1-14C]acetate (Fig. 1C).
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Distribution of radioactivity between polar acyl lipids and other chloroform-extractable compounds
In leaf tissue, acetate is used as a substrate for the synthesis of fatty acids, chlorophyll and carotenoids in chloroplasts and of sterols in the endoplasmic reticulum (Goodwin and Mercer, 1988). To determine the proportion of [1-14C]acetate allocated to membrane-forming acyl lipids, the lipid extracts were subfractionated by TLC.
The proportion of the total lipid-associated radioactivity retrieved in phospholipids and galactolipids was markedly lower in the second oldest leaflet from plants that were 14–22-d-old when labelled, than in the corresponding leaflet from the oldest plants (Fig. 2).
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Kinetics of radiolabel incorporation into polar acyl lipids and free sterols
To determine whether allocation of [1-14C]acetate into different lipid classes varied during the life-span of a leaf, the kinetics of radioactivity incorporation into PC, PG, MGDG, DGDG, PE, and free sterols into the second-oldest leaf of pea plants that were 10, 22 and 40-d-old when labelled were analysed. Leaves were sampled for lipid extraction 4, 24 and 72 h after radiolabelling. In the still expanding leaf of the 10-d-old plants (Fig. 3A, B), acetate allocation into the lipid classes analysed was 3–4 times greater than in the older plants. Four hours after radiolabelling, PC was the major radiolabelled lipid, but the proportion (Fig. 3A) of radioactivity associated with PC decreased during the remainder of the time analysed. Concomitantly with this decrease, the radioactivity associated with the galactolipids, primarily MGDG, increased. Acetate allocation into PG, PE and free sterols were all relatively low and peaked before the last sampling occasion (absolute data not shown). Thus, in the still expanding leaf of the 10-d-old plants, only the chloroplast galactolipids continued to incorporate radiolabel throughout the 3 d.
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) PG; (
) DGDG; (
) MGDG. (B, D, F) (
) PE; (In the plants that were 22-d-old when radiolabelled, all lipids except free sterols continued to incorporate radioactivity during the 3 d studied, although all lipids except PG incorporated less radioactivity during the 3 d of incubation, compared to the 10-d-old plants (absolute data not shown). In contrast to the younger plant, PC was not the lipid initially most highly radiolabelled but PG, which also remained the most radioactive lipid 72 h after radiolabelling (Fig. 3C
, D). As in the younger plants, MGDG and DGDG radioactivity as well as their proportions of lipid radioactivity increased with time, but in the 22-d-old plants, the increase was moderate and the proportions of radioactivity were always below those of PC and PG. Compared to the youngest plant, a larger proportion of the radioactivity was associated with PE, whereas the proportion of radiolabel associated with the free sterols were similar between the two plant ages.
In the 40-d-old plants (Fig. 3E, F), radiolabel incorporation into PC, PG and MGDG was initially markedly faster than in the 22-d-old plants (absolute data not shown), but for PC and PG, similar magnitudes as in these younger plants were reached after 72 h. The galactolipids continued to incorporate radioactivity through the 72 h period.
Distribution of radioactivity between different membrane lipid classes
To study the influence of leaf age on the pattern of acetate utilization for lipid synthesis in more detail, the proportion of the total lipid extract radioactivity associated with each of the lipid classes MGDG, DGDG, PC, PE, PG, and free sterols were compared 4, 24 and 72 h after radiolabelling of the second oldest leaf of plants aged between 10 and 40-d-old when labelled.
Four hours after radiolabelling (Fig. 4A–C), PC was the most radioactive lipid in the youngest plants, containing around 33% of the radiolabel, but its proportion of the total lipid radiolabel decreased with increased plant age to reach a minimum value of around 15% in 26-d-old plants. In older plants, the proportion of radiolabel in PC again increased. During the first 4 h after labelling, PG incorporated less than 10% of the lipid-associated radiolabel in the youngest plant, but 25–27% in leaves of intermediary age, where it was the most radioactive lipid. In leaves from the older plants (30–40-d-old), the proportions of radioactivity associated with PG and PC 4 h after radiolabelling were similar around 22% each in the 30-d-old plants and close to 30% in the 40-d-old plants. MGDG incorporated less than 10% of the radioactivity during the first 4 h in all plant ages and the label showed a similar pattern as described for PC, that is, a decrease in radioactivity with increasing plant age followed by an increase in the oldest plants. Incorporation of radioactivity into DGDG was very low in all plant ages and there were no clear plant age-dependent variations in the proportions of radioactivity early incorporated into DGDG, PE or free sterols.
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Twenty-four hours after radiolabelling (Fig. 4D
–F), in the expanding leaflet of the 10-d-old plants, the highest proportion of radioactivity was no longer associated with PC (11%) but with MGDG (22%). In leaves from 18- or 22-d-old plants, MGDG contained only around 5% of the lipid radioactivity, but in the older plants, the proportion of lipid radioactivity allocated into MGDG increased with plant age. The labelling of DGDG exhibited an age-dependent pattern similar to that of MGDG, although at a much lower radioactivity level. In the 18–40-d-old plants, PG was the most radioactive lipid, containing around 25% of the radioactivity. The lowest proportion of radioactivity retrieved in PG, was, as with PC, found in the youngest plants. PE contained 7–11% of the radioactivity in plants that were 14–22-d-old when labelled. The highest fraction of lipid radioactivity associated with free sterols was in 18-d-old plants, and it decreased with increased plant age.
Seventy-two hours after radiolabelling (Fig. 4G–I), the distribution of radioactivity among the lipid classes of plants of different ages resembled the situation obtained after 24 h, although the trends were more pronounced. The main differences were that PE retained a higher proportion of radioactivity in the older plants 72 h after radiolabelling than after 24 h and that the proportion of radioactivity associated with free sterols clearly decreased with increased plant age.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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These results clearly demonstrate the dynamics inherent in membrane lipid metabolism during the life span of a pea leaf. Fatty acid synthesis was most active in the still expanding leaf of the 10-d-old peas. Three days after radiolabelling, 30–35% of the added acetate was associated with galactolipids and the major phospholipids (calculated from recovered radioactivity and data in Figs 1
and 2). Once the leaf was fully expanded, fatty acid synthesis proceeded at a lower but stable rate during the remainder of the leaf life-time analysed, including when the first signs of tissue degradation had become visible. In these leaves the galactolipids and major phospholipids retained around 10% of the added radioactivity. The leaf age differences in utilization of the added [1-14C]acetate for fatty acid synthesis could reflect different dilution with endogenous acetate. However, it has been reported that the cellular pool of free acetate is higher in younger than in older garden pea leaves (Roughan, 1995). Thus, these results would have underestimated fatty acid synthesis in younger leaves compared to the older ones, if the administered radiolabelled acetate had equilibrated with the free acetate pool. The conclusion that fatty acid synthesis was higher in the still expanding leaves than in the fully expanded leaves thus still stands. In addition, it was recently suggested that the bulk pool of cellular acetate is not involved in fatty acid synthesis (Bao et al., 2000). When interpreting the results of this study, it should be noted that radiolabelling of acyl lipids does not exclusively reflect de novo synthesis of the entire lipid molecule, but rather reflects the renewal of the fatty acids within the lipid class, either through neo-synthesis of the entire acyl lipid or by incorporation of newly synthesized fatty acids into pre-existing acyl lipids.
In the still expanding leaf, the fatty acids during the first hours were predominantly allocated into PC, reflecting that most of the newly synthesized fatty acids were exported for lipid synthesis outside the chloroplast. The continued incorporation of radiolabel occurred mainly into the galactolipids, reflecting the requirement for membrane material as chloroplast numbers and thylakoid area increased. The concomitant decrease in PC radioactivity and the increase in galactolipid radioactivity, together with the fact that DAG never contained more than 1% of the lipid-associated radioactivity, support the proposed precursor role for PC or PC derivatives in galactolipid synthesis (Mongrand et al., 1997, 2000).
In the fully expanded leaves, all the acyl lipids studied continued to incorporate acetate-derived radiolabel during the 3 d analysed. In these leaves, PG, not MGDG, was the most heavily radiolabelled lipid. MGDG contained only around 10% of the lipid radiolabel in fully expanded second-oldest leaves, compared to around 42 mol% of the lipids in corresponding pea leaves (Carlsson et al., 1994). The results indicate that the acyl chains of the galactolipid component of the recently fully expanded leaves are relatively stable. However, in older plants, allocation of radiolabel into MGDG increased. As the MGDG content of the second-oldest leaves of garden pea has been reported to remain constant until the plants were at least 40-d-old (Olsson, 1995), the result may reflect an increased need for thylakoid repair. The leaves started to show signs of senescence on day 40, but they still increased the incorporation of radiolabel into MGDG compared with the leaves on plants of intermediate age.
In the fully expanded leaves, PG contained more than 20% of the leaf lipid radioactivity, whereas it was reported to constitute only 7 mol% of the acyl lipids (Carlsson et al., 1994). Assuming that the radiolabelled PG represented chloroplast PG, a larger proportion of PG radioactivity than of PG amount in the expanded leaves could be explained either by a higher rate of turnover or acyl group exchange of PG than of the other acyl lipids, or that phospholipid synthesis in the endoplasmic reticulum to a larger extent than PG synthesis in the chloroplast utilized acyl groups formed prior to radiolabelling. If such an isotope dilution had occurred in the cytoplasmic lipid synthesis, a lower proportion of PE labelling than its mass proportion would have been expected. However, 3 d after radiolabelling, PE in 18–26-d-old plants contained around 10% of the lipid radioactivity, whereas PE was reported to constitute 6–7 mol% of the acyl lipids of second oldest leaf of 14–23-d-old pea plants (Carlsson et al., 1994). Thus, a higher rate of turnover for chloroplastic PG than for MGDG is the most likely explanation for the obtained results. Whether this represents a higher turnover of the entire PG molecule, or only acyl chain turnover, cannot be deduced from the present work. Both MGDG and PG have been shown to be associated with the light harvesting complex II (Remy et al., 1982; Tremolieres et al., 1994). However, in the cyanobacteria Oscillatoria chalybea, PG is more tightly associated with the highly turned-over D1 subunit of PSII than MGDG (Kruse and Schmidt, 1995), and in Synechocystis sp. PCC6803 mutants defective in PG synthesis, PG supplementation was required for growth and normal functioning of PSII (Hagio et al., 2000; Sato et al., 2000). These results suggest that PG is in closer proximity to the highly oxidative photochemical processes than MGDG, which would also explain the higher turnover rate of acyl chains in PG, compared with MGDG.
Most previous investigations have employed monocotyledon species and short incubation times. Nevertheless, with expanded leaf tissue, a 2–3-fold higher incorporation of [14C]acetate into PG than into MGDG has usually been reported, for example, in maize (Slack and Roughan, 1975 [2.5 h incubation time]; Bolton and Harwood, 1978 [2 h]), wheat (Bolton and Harwood, 1978 [2 h]; O'Sullivan and Dalling, 1989 [1–36 h]; Williams et al., 1998a, b [4 h]), and rye (Bolton and Harwood, 1978 [2 h]). With barley, however, all leaf segments, from the basal one to those from fully expanded tissue, incorporated more [14C]acetate into MGDG than into PG, although the ratio of radiolabelled MGDG to radiolabelled PG decreased with increased tissue age (Bolton and Harwood, 1978 [2 h]). As the ratio of radiolabel to lipid mass was higher in PG than in MGDG in all leaf sections, the results also indicate a less stable PG than MGDG in this plant species, as well as in the other monocotyledons investigated.
In previous investigations on ageing or senescent leaves, the contents of galactolipids and phospholipids were found to decrease, but the different lipid classes did not decrease simultaneously. In both bean (Fong and Heath, 1977) and wheat (Sandelius et al., 1995), degradation or discontinued replacement occurred earlier with chloroplast lipids than with phospholipids and the leaf content of PE actually continued to increase until the very last stages of senescence. The decrease in phospholipids during leaf senescence usually results in an increased ratio of free sterols to phospholipids (McKersie et al., 1978). A comparison of acetate allocation into total phospholipid relative to that of free sterols cannot be made, as the radiolabelled PG mainly reflected chloroplast PG and radiolabelled PC partly reflected its transient role in galactolipid synthesis. However, a continued incorporation of fatty acids in PE was observed and also that synthesis of free sterols decreased earlier than the radiolabelling of PE. These data do not report on the actual mass relationships between free sterols and phospholipids but, nevertheless, indicates that the observed change in the phospholipid/free sterol ratio during senescence is not due to a markedly increased rate in the synthesis of free sterols.
To conclude, the results clearly demonstrate the transient variations in channelling the capacity for lipid synthesis towards different lipid classes and probably different membranes during the life-span of a leaf. Furthermore, these data point to the need for identifying the lipid metabolic stage of the tissue when investigating lipid metabolism.
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Acknowledgments |
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Financial support was from the Swedish Natural Science Research Council and the Swedish Council for Forestry and Agricultural Research.
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Notes |
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1 Present address and to whom correspondence should be sent: Biocentrum-DTU, Technical University of Denmark, Søltofts Plads, Building 224, DK-2800 Lyngby, Denmark. Fax: +45 45886307. E-mail: lars.hellgren{at}biocentrum.dtu.dk
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Abbreviations |
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DAG, diacylglycerol; DGDG, digalactosyldiacylglycerol; MGDG, monogalactosyldiacylglycerol; PC, phosphatidylcholine; PE, phosphatidylethanolamine; PG, phosphatidylglycerol.
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