Phosphate‐deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol

Andersson, Mats X.; Stridh, Malin H.; Larsson, Karin; Liljenberg, Conny; Sandelius, Anna Stina

doi:10.1016/s0014-5793(03)00109-1

Cited by 256 publications

(219 citation statements)

References 29 publications

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“…Under these conditions, particularly high amounts of DGDG were found in roots that lack chloroplasts, and fractionation experiments were consistent with the accumulation of DGDG in extraplastidic membranes following phosphate deprivation. The presence of small amounts of galactoglycerolipids in the plasma membrane or the tonoplast (vacuolar membrane) has been described previously (39 -41), and recent reexamination of this issue has now firmly established that phosphate deprivation induces the accumulation of DGDG in plasma membranes (42)(43)(44), possibly to substitute for bilayer-forming phospholipids (4,45). Moreover, DGDG has been found in the peribacteroid membrane of legume root nodules (46), and it is also a major glycolipid of non-photosynthetic floral organs in petunia (47).…”

Section: Minireview: Plant Galactoglycerolipid Biosynthesis 2398mentioning

confidence: 66%

Three Enzyme Systems for Galactoglycerolipid Biosynthesis Are Coordinately Regulated in Plants

Benning

Ohta

2005

Journal of Biological Chemistry

195

148

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Galactoglycerolipids, in which galactose is bound at the glycerol sn-3 position in O-glycosidic linkage to diacylglycerol, are abundant in plants and photosynthetic bacteria, where they constitute the bulk of the polar lipids of the photosynthetic membranes. Galactoglycerolipid biosynthesis in plants is highly compartmentalized involving enzymes at the endoplasmic reticulum and the two chloroplast envelopes. This peculiar organization requires extensive trafficking of lipid precursors. It is now increasingly apparent that there are three different sets of lipid galactosyltransferases capable of galactoglycerolipid biosynthesis in the model plant Arabidopsis. Two enzymes, MGD1 and DGD1, provide the bulk of galactoglycerolipids in the chloroplast and in photosynthetic tissues in general. Under phosphate-limited growth conditions and in non-photosynthetic tissues MGD2/3 and DGD2 are highly active. Moreover, galactoglycerolipids produced by this second pathway are often found in extraplastidic membranes. Although these galactosyltransferases use UDP-Gal as the galactose donor, a third pathway involves a processive enzyme, which transfers galactose from one galactolipid to another.In thinking about membrane lipids, phosphoglycerolipids often come to mind first as these are the primary building blocks of many eukaryotic and prokaryotic cell membranes. However, in plant cells the fraction of phosphoglycerolipids is relatively small. Instead, non-phosphorous galactoglycerolipids are predominant, representing up to 50% of polar lipids in extracts of photosynthetic tissues (1). Of the different galactolipids reported for plants (2), most abundant are the monogalactosyldiacylglycerol (MGDG) 1 and digalactosyldiacylglycerol (DGDG) lipids (cf. Fig. 1 for structures). In addition, under certain circumstances, e.g. in the Arabidopsis tgd1 mutant (3), plants can synthesize higher galactosylated forms of galactoglycerolipids. Although most of these lipids are restricted to the chloroplast membranes in plants, it has become increasingly apparent that galactoglycerolipids are present in extraplastidic membranes in non-photosynthetic tissues or under phosphate-limited growth conditions (4). Current evidence suggests that galactoglycerolipids are exclusively synthesized by enzymes associated with the two chloroplast envelopes in plants, a fact that requires the transfer of lipid precursors to, between, and through the envelopes as well as that of galactoglycerolipids from the envelopes to the photosynthetic membranes inside the chloroplast (thylakoids) and to extraplastidic membranes (5). The three classes of glycosyltransferases ( Fig. 1) involved in galactoglycerolipid biosynthesis in plants and their respective functions and interactions in vivo will be discussed. Monogalactosyldiacylglycerol SynthasesThe most abundant plant galactoglycerolipid, 1␤-MGDG, is synthesized in plants by the action of a galactosyltransferase (MGDG synthase, EC 2.4.1.46) catalyzing the transfer of a galactosyl residue from UDP-1␣-Gal to the sn-3-posit...

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Section: Minireview: Plant Galactoglycerolipid Biosynthesis 2398mentioning

confidence: 66%

Three Enzyme Systems for Galactoglycerolipid Biosynthesis Are Coordinately Regulated in Plants

Benning

Ohta

2005

Journal of Biological Chemistry

195

148

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“…see Ref. 25) particularly in highly purified plant PM (26). Sphingolipid was found to be the major nonglycerolipid in leaf PM (21.1 Ϯ 2.3% of total lipid) but represented 2-fold less in BY2 cell PM (Fig.…”

Section: Isolation Of Detergent-insoluble Membranes From Tobaccomentioning

confidence: 84%

Lipid Rafts in Higher Plant Cells

Mongrand

Morel

Laroche

et al. 2004

Journal of Biological Chemistry

423

119

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A large body of evidence from the past decade supports the existence of functional microdomains in membranes of animal and yeast cells, which play important roles in protein sorting, signal transduction, or infection by pathogens. They are based on the dynamic clustering of sphingolipids and cholesterol or ergosterol and are characterized by their insolubility, at low temperature, in nonionic detergents. Here we show that similar microdomains also exist in plant plasma membrane isolated from both tobacco leaves and BY2 cells. Tobacco lipid rafts were found to be greatly enriched in a sphingolipid, identified as glycosylceramide, as well as in a mixture of stigmasterol, sitosterol, 24-methylcholesterol, and cholesterol. Phospho-and glycoglycerolipids of the plasma membrane were largely excluded from lipid rafts. Membrane proteins were separated by oneand two-dimensional gel electrophoresis and identified by tandem mass spectrometry or use of specific antibody. The data clearly indicate that tobacco microdomains are able to recruit a specific set of the plasma membrane proteins and exclude others. We demonstrate the recruitment of the NADPH oxidase after elicitation by cryptogein and the presence of the small G protein NtRac5, a negative regulator of NADPH oxidase, in lipid rafts.A new aspect of the lipid bilayer organization has arisen from biophysical and biochemical studies performed with animal cells for several years. Indeed, lipids are not uniformly miscible, but lateral separation of specific lipid species leads to the formation of specialized phase domains also called "lipid rafts" (1). The main role in the process of domain organization is played by sterols and sphingolipids, these latter interacting together through weak interaction between aliphatic chains stabilized by the presence of saturated alkyl chains, voids between sphingolipids being filled by sterols (for a review, see Ref.2). The cholesterol-sphingolipid-enriched domain formation is also enhanced by the fact that sphingolipids have higher melting temperatures than phospholipids. Regions between rafts are occupied by phospholipids, with unsaturated fatty acids forming a liquid-crystalline phase, whereas lipid rafts that contain more saturated aliphatic chains form a liquidordered phase. In model and biological membranes, the formation of the liquid-ordered phase correlates with resistance to solubilization by nonionic detergent such as Triton X-100 at 4°C and buoyancy at specific density in a sucrose gradient (3). Thus, isolation of detergent-insoluble membranes (DIM) 1 or detergent-insoluble glycolipid-enriched membrane domains is one of the most widely used methods for studying lipid rafts.In animal cells, these membrane domains act, for example, as sorting devices for the accumulation of acylated, glycosylphosphatidylinositol-anchored, palmitoylated signaling molecules that selectively locate in these domains. Tyrosine kinases of the Src family protein, heterotrimeric and small G-proteins, as well as phosphoinositides have been proved to be...

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“…To cope with limiting Pi conditions plants activate diverse mechanisms that allow them to increase Pi availability, uptake, and utilization (1-7). One of the biochemical mechanisms that plants activate to recycle Pi from storage compounds during Pi deprivation is the hydrolysis of phospholipids (8)(9)(10).…”

Section: Discussionmentioning

confidence: 99%

“…A concomitant increase in the synthesis of nonphosphorus lipids such as the galactolipid digalactosyldiacylglycerol (DGDG) and the sulfolipid sulfoquinovosyldiacylglycerol (SQDG) occurs presumably to preserve membrane integrity (8)(9)(10). Although DGDG is typically found in plastid membranes, during Pi deprivation it has been proposed that DGDG replaces phospholipids in the plasma membrane.…”

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confidence: 99%

Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots

Cruz‐Ramírez¹,

Oropeza-Aburto²,

Razo-Hernández³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

245

232

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Low phosphate (Pi) availability is one of the major constraints for plant productivity in natural and agricultural ecosystems. Plants have evolved a myriad of developmental and biochemical mechanisms to increase internal Pi uptake and utilization efficiency. One important biochemical pathway leading to an increase in internal Pi availability is the hydrolysis of phospholipids. Hydrolyzed phospholipids are replaced by nonphosphorus lipids such as galactolipids and sulfolipids, which help to maintain the functionality and structure of membrane systems. Here we report that a member of the Arabidopsis phospholipase D gene family (PLDZ2) is gradually induced upon Pi starvation in both shoots and roots. From lipid content analysis we show that an Arabidopsis pldz2 mutant is defective in the hydrolysis of phospholipids and has a reduced capacity to accumulate galactolipids under limiting Pi conditions. Morphological analysis of the pldz2 root system shows a premature change in root architecture in response to Pi starvation. These results show that PLDZ2 is involved in the eukaryotic galactolipid biosynthesis pathway, specifically in hydrolyzing phosphatidylcholine and phosphatidylethanolamine to produce diacylglycerol for digalactosyldiacylglycerol synthesis and free Pi to sustain other Pi-requiring processes.phosphate starvation ͉ phospholipids ͉ root architecture ͉ sulfolipids P hosphate (Pi) influences virtually all developmental and biochemical processes in plants. Pi is not only a constituent of key cell molecules such as ATP, nucleic acids, and phospholipids, but it is also a pivotal metabolic regulator of many processes including energy transfer, protein activation, and carbon and nitrogen metabolism. However, Pi availability can be one of the major constraints for plant growth in both natural and agricultural ecosystems because of its low mobility and high absorption capacity in the soil. As a response to this limitation, plants have evolved a range of developmental, biochemical, and symbiotic adaptive strategies to cope with low Pi availability (1, 2). In Arabidopsis, a general, 3-fold strategy to cope with low Pi availability has been described. (i) The release and uptake of Pi from external sources that are not readily available for plant uptake. This mechanism includes the transcriptional activation of high-affinity Pi transporters and the excretion of RNases, acid phosphatases, and organic acids (3-5). (ii) Changes in the architecture of the root system that reflect alterations in cell length, root meristem activity, root hair elongation, and an increased number of lateral roots (6, 7). These changes presumably increase the exploratory capacity of the root and the absorptive surface area. (iii) Optimization of Pi utilization due to a wide range of metabolic alterations, and the mobilization of Pi from internal reserves by the hydrolysis of nucleic acids, proteins, and the recycling of Pi from membrane phospholipids.During Pi deprivation, the total content of diverse phospholipids such as phosphatidylcholin...

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Phosphate‐deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol

Cited by 256 publications

References 29 publications

Three Enzyme Systems for Galactoglycerolipid Biosynthesis Are Coordinately Regulated in Plants

Three Enzyme Systems for Galactoglycerolipid Biosynthesis Are Coordinately Regulated in Plants

Lipid Rafts in Higher Plant Cells

Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots

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