Photosynthetic Membrane Lipids Research Articles

Arabidopsis as a genetic model for interorganelle lipid trafficking.

In eukaryotic cells the biosynthesis of membrane lipids often occurs in subcellular compartments different from their final destination. This raises a fundamental question: How are membrane lipids transported between organelles and across membranes? The intricate compartmentalization of plant lipid metabolism provides promising opportunities for the mechanistic analysis of interorganelle lipid trafficking. In plants the endoplasmic reticulum (ER) and the chloroplast envelopes participate in the biosynthesis of the lipids of photosynthetic membranes. As a consequence, trafficking of lipid precursors between these two membrane systems is substantial. As will be discussed below, Arabidopsis represents an excellent plant model to dissect this process genetically and may provide experimental access to a better mechanistic understanding of interorganelle lipid trafficking in general.

Novel polar lipids of halophilic eubacterium Planococcus H8 and archaeon Haloferax volcanii

As part of a study to identify novel lipids with immune adjuvant activity, a structural comparison was made between the polar lipids from two halophiles, an archaeon Haloferax volcanii T and a eubacterium Planococcus H8. H. volcanii polar lipid extracts consisted of 44% archaetidylglycerol methylphosphate, 35% archaetidylglycerol, 4.7% of archaeal cardiolipin, 2.5% archaetidic acid, and 14% sulfated glycolipids 1 and 2. Nuclear magnetic resonance (NMR) and Fast atom bombardment mass spectrometry (FAB MS) data determined the glycolipids to be 6-HSO 3- d-Man p-α1-2- d-Glc p-α1,1-[ sn-2,3-di- O-phytanylglycerol] and a novel glycocardiolipin 6′-HSO 3- d-Man p-α1-2- d-Glc p-α1,1-[ sn-2,3-di- O-phytanylglycerol]-6-[phospho- sn-2,3-di- O-phytanylglycerol]. The polar lipids of Planococcus H8 consisted of 49% saturated phosphatidylglycerol and cardiolipin (9:1, w/w), and surprisingly 51% of the photosynthetic membrane lipid sulfoquinovosyldiacylglycerol (SQDG). This study documents archaeal cardiolipin and a novel glycocardiolipin in H. volcanii (lacking purple membrane), and is the first report of SQDG in a non-photosynthetic, halophilic bacterium.

A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis.

In eukaryotes, enzymes of different subcellular compartments participate in the assembly of membrane lipids. As a consequence, interorganelle lipid transfer is extensive in growing cells. A prominent example is the transfer of membrane lipid precursors between the endoplasmic reticulum (ER) and the photosynthetic thylakoid membranes in plants. Mono- and digalactolipids are typical photosynthetic membrane lipids. In Arabidopsis, they are derived from one of two pathways, either synthesized de novo in the plastid, or precursors are imported from the ER, giving rise to distinct molecular species. Employing a high-throughput robotic screening procedure generating arrays of spot chromatograms, mutants of Arabidopsis were isolated, which accumulated unusual trigalactolipids. In one allelic mutant subclass, trigalactosyldiacylglycerol1, the primary defect caused a disruption in the biosynthesis of ER-derived thylakoid lipids. Secondarily, a processive galactosyltransferase was activated, leading to the accumulation of oligogalactolipids. Mutations in a permease-like protein of the outer chloroplastic envelope are responsible for the primary biochemical defect. It is proposed that this protein is part of a lipid transfer complex.

Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth.

The sulfolipid sulfoquinovosyldiacylglycerol is one of the three nonphosphorous glycolipids that provide the bulk of the structural lipids in photosynthetic membranes of seed plants. Unlike the galactolipids, sulfolipid is anionic at physiological pH because of its 6-deoxy-6-sulfonate-glucose (sulfoquinovose) head group. The biosynthesis of this lipid proceeds in two steps: first, the assembly of UDP-sulfoquinovose from UDP-glucose and sulfite, and second, the transfer of the sulfoquinovose moiety from UDP-sulfoquinovose to diacylglycerol. The first reaction is catalyzed by the SQD1 protein in Arabidopsis. Here we describe the identification of the SQD2 gene of Arabidopsis. We propose that this gene encodes the sulfoquinovosyltransferase catalyzing the second step of sulfolipid biosynthesis. Expression of SQD1 and SQD2 in Escherichia coli reconstituted plant sulfolipid biosynthesis in this bacterium. Insertion of a transfer DNA into this gene in Arabidopsis led to complete lack of sulfolipid in the respective sqd2 mutant. This mutant showed reduced growth under phosphate-limited growth conditions. The results support the hypothesis that sulfolipid can function as a substitute of anionic phospholipids under phosphate-limited growth conditions. Along with phosphatidylglycerol, sulfolipid contributes to maintaining a negatively charged lipid-water interface, which presumably is required for proper function of photosynthetic membranes.

Thermal stability of oxygen evolution in photosystem ? core complex in the presence of digalactosyl diacylglycerol

The influence of digalactosyldiacylglycerol (DGDG), one of the photosynthetic membrane lipids, on heat inactivation of the process of oxygen evolution has been studied in vitro in photosystem II (PS II) core complex. It was found that the temperature of semi-inactivation of oxygen evolution in the complex increased from 40.0 to about 43.0°C in the presence of DGDG with 5-min heat treatment in the dark. Furthermore, when PS II core complex was incubated for 5 min at 45.0°C, the oxygen evolution in the complex was completely lost, whilst the DGDG-complexed PS II core complex still retained a 16% of activity (100% for 25.0°C). In addition, a 1-h incubation at 38.0°C inactivated absolutely the oxygen evolution for the PS II core complex. By contrast, there remained about 20% of activity (zero time for 100%) for the complex in the presence of DGDG under the same condition. These results indicate a new role of DGDG in the protection of PS II core complex against the deleterious effects of temperature. It was most likely that DGDG-mediated stability toward thermal denaturation of oxygen evolution in PS II core complex is due to the protective effect of DGDG on the release of the 33 kD protein from PS II core complex.

Digalactosyl diacylglycerol-mediated Stability toward Thermal Denaturation of Oxygen Evolution in Photosystem II Core Complex

The influence of digalactosyldiacylglycerol (DGDG), one of the photosynthetic membrane lipids, on heat inactivation of the process of oxygen evolution has been studied in vitro in photosystem II (PSII) core complex. It was found that the temperature of semi-inactivation of oxygen evolution in the complex increased from 40 to about 43 degrees C in the presence of DGDG. Furthermore, when incubated for 5 min at 45° C, the oxygen evolution in PSII core complex was completely lost, whilst DGDG-complexed PSII core complex still retained a 16% of activity (100% for 25° C). In addition, a one-hour incubation at 38° C inactivated absolutely the oxygen evolution for the PSII core complex. By contrast, there remained about 20% of activity (zero time for 100%) for the complex in the presence of DGDG on the same condition. These results might indicate the role of DGDG in the protection of PSII core complex against the deleterious effects of temperature. It was suggested that the DGDG-mediated stability toward thermal denaturation of oxygen evolution in PSII core complex is due to the redistribution of secondary bonds in PSII core complex proteins through interactions with the polar and/or fatty acid parts of DGDG, which results in DGDG-induced restraint on the inhibitory effect of heat.

Virus impact upon bean plant photosynthesising tissue lipid composition

Study of bean plants infected by tabacco mosaic virus and potato X virus was performed. Virus infection of bean plants induced the injury of structural state of photosynthetic apparatus, viz., the a/b chlorophyll ratio decreased and the main photosynthetic membrane lipid monogalactosyl diacylglycerol degradation took place with parallel accumulation of intermediate compound suggested to perform a signal function. Phospholipid and free sterol content increase pointed out on the changes of the membrane fluidity and permeability. Accumulation of sulphoquinovosyl diacylglycerol in infected plants evidences the probability of latter to play important roles in adaptive reactions of photosynthetic apparatus.

The phase behavior of lipids in photosynthetic membranes.

The phase behavior of the main classes of polar lipids found in the photosynthetic membranes of higher plants and algae is reviewed and compared to that of binary lipid mixtures and total lipid extracts of such membranes. Particular interest is paid to the way in which factors such as temperature and acyl chain saturation influence the phase behavior of these lipids and the implications this has in terms of the ability of photosynthetic membranes to resist environmental stress.

The effects of galactolipid depletion on the structure of a photosynthetic membrane.

The galactolipids monogalactosyldiglyceride and digalactosyldiglyceride together comprise more than 77% of the photosynthetic membrane lipids of higher plant chloroplasts. We have isolated a lipase from the chloroplasts of runner beans (Phaseolus vulgaris) which is highly specific for these galactolipids. This galactolipase promotes the hydrolysis of monogalactosyldiglyceride and digalactosyldiglyceride, in the process liberating two free fatty acids into the membrane bilayer, leaving the residual galactosyl glyceride group to diffuse into the aqueous bulk phase. Isolated spinach photosynthetic membranes were treated with this enzyme preparation and changes in membrane composition were studied with thin layer chromatography (for lipids), gel electrophoresis (proteins), and freeze-etching (membrane structure). After 30 min of lipolysis, nearly 100% of the galactolipids had been converted into membrane-associated fatty acids and water-soluble galactosyl glycerides. SDS PAGE showed that two proteins, one of which is possibly associated with the reaction center of photosystem II, were removed by the treatment. Despite the minor nature of changes in membrane protein composition, freeze-fracture and freeze-etch studies showed that striking changes in membrane structure had taken place. The large freeze-fracture particle on the E fracture face had disappeared in stacked regions of the membrane system. In addition, a tetrameric particle visible at the inner surface of the membrane had apparently dissociated into individual monomeric particles. The fact that these two structures are so dramatically affected by the loss of galactolipids strongly suggests that these lipids play a crucial role in maintaining their structure. Both structures are believed to be different views of the same transmembrane unit: a membrane-spanning complex associated with photosystem II. Our results are consistent with two possible interpretations: the intramembrane particles may be lipidic in nature, and hence lipolysis causes their disappearance; or galactolipids are necessary for the organization of a complex photosystem II-associated structure which is composed of a number of different molecular species.

The structural role of lipids in photosynthetic membranes

The structural role of lipids in photosynthetic membranes