Evolution of galactoglycerolipid biosynthetic pathways – From cyanobacteria to primary plastids and from primary to secondary plastids

Petroutsos, Dimitris; Amiar, Souad; Abida, Heni; Dolch, Lina-Juana; Bastien, Olivier; Rébeillé, Fabrice; Jouhet, Juliette; Falconet, Denis; Block, Maryse A.; McFadden, Geoffrey I.; Bowler, Chris; Botté, Cyrille Y.; Maréchal, Éric

doi:10.1016/j.plipres.2014.02.001

Cited by 126 publications

(144 citation statements)

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“…Sequence alignment and details are given in Supplemental Figure S1. and TAGs are instead synthesized in the ER (Petroutsos et al, 2014). Based on genomic evidence, the metabolic pathways for the production of glycerolipids are expected to follow this general scheme in Nannochloropsis.…”

Section: Regulation Of Genes Involved In Lipid Metabolismmentioning

confidence: 99%

Light Remodels Lipid Biosynthesis in Nannochloropsis gaditana by Modulating Carbon Partitioning between Organelles

et al. 2016

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The seawater microalga Nannochloropsis gaditana is capable of accumulating a large fraction of reduced carbon as lipids. To clarify the molecular bases of this metabolic feature, we investigated light-driven lipid biosynthesis in Nannochloropsis gaditana cultures combining the analysis of photosynthetic functionality with transcriptomic, lipidomic and metabolomic approaches. Light-dependent alterations are observed in amino acid, isoprenoid, nucleic acid, and vitamin biosynthesis, suggesting a deep remodeling in the microalgal metabolism triggered by photoadaptation. In particular, high light intensity is shown to affect lipid biosynthesis, inducing the accumulation of diacylglyceryl-N,N,N-trimethylhomo-Ser and triacylglycerols, together with the up-regulation of genes involved in their biosynthesis. Chloroplast polar lipids are instead decreased. This situation correlates with the induction of genes coding for a putative cytosolic fatty acid synthase of type 1 (FAS1) and polyketide synthase (PKS) and the down-regulation of the chloroplast fatty acid synthase of type 2 (FAS2). Lipid accumulation is accompanied by the regulation of triose phosphate/inorganic phosphate transport across the chloroplast membranes, tuning the carbon metabolic allocation between cell compartments, favoring the cytoplasm, mitochondrion, and endoplasmic reticulum at the expense of the chloroplast. These results highlight the high flexibility of lipid biosynthesis in N. gaditana and lay the foundations for a hypothetical mechanism of regulation of primary carbon partitioning by controlling metabolite allocation at the subcellular level.

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Section: Regulation Of Genes Involved In Lipid Metabolismmentioning

confidence: 99%

Light Remodels Lipid Biosynthesis in Nannochloropsis gaditana by Modulating Carbon Partitioning between Organelles

et al. 2016

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“…structure (Carter et al, 1956;Boudière et al, 2014;Petroutsos et al, 2014). Although chloroplasts directly synthesize MGDG from diacylglycerol and UDP-galactose (Shimojima et al, 1997), cyanobacteria first convert diacylglycerol and UDP-glucose…”

Section: Biosynthesis Of Galactolipids In Oxygenic Phototrophsmentioning

confidence: 99%

Configuration of the sugar head of glycolipids in thylakoid membranes

Apdila

Awai

2017

Genes Genet. Syst.

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Glycolipids constitute the majority of membrane components in oxygenic photosynthetic organisms, whereas they are minor lipids in other organisms. In cyanobacteria, three glycolipids comprise ~90 mol% of the total lipids in thylakoid membranes, where photosynthetic electron transport occurs. Among these glycolipids, 80 mol% are galactolipids (monogalactosyldiacylglycerol and digalactosyldiacylglycerol). Galactolipids are well conserved in oxygenic photosynthetic organisms and are believed to be essential for the integrity of the membrane system. It remains unclear, however, which part(s) of the galactolipid structure is the key factor for their function, e.g., the sugar moiety and/or the anomeric configuration. To address this issue, several bacterial membrane glycolipid synthase genes have been introduced into cyanobacteria to test for complementation of knocked-out genes involved in galactolipid biosynthesis. In this review, we summarize recent advances in the analyses of sugar species and configurations of glycolipids heterologously synthesized in the thylakoid membrane and discuss their functional importance.4

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“…CDGD1/DGD2-like sequences are found in all Streptophyta and in some Chlorophyta and Rhodophyta (SI Appendix, Figs. S1 and S2) (16). Spermatophyta contain two sequences, DGD1 and DGD2, with only DGD1 encompassing the NDGD1 extension (SI Appendix, Fig.…”

Section: Significancementioning

confidence: 99%

“…Other Chlorophyta (Chlorella, Auxenochlorella, and Micromonas) contain only a single DGD2 gene without the extension. Within Rhodophyta, Chondrus contains a single DGD2-like gene (16), and Porphyridium contains two genes, a DGD1-like sequence and a DGD2 sequence (SI Appendix, Figs. S1 and S2).…”

Section: Significancementioning

confidence: 99%

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Synthesis and transfer of galactolipids in the chloroplast envelope membranes of Arabidopsis thaliana

Kelly

Kalisch

Hölzl

et al. 2016

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

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Galactolipids [monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG)] are the hallmark lipids of photosynthetic membranes. The galactolipid synthases MGD1 and DGD1 catalyze consecutive galactosyltransfer reactions but localize to the inner and outer chloroplast envelopes, respectively, necessitating intermembrane lipid transfer. Here we show that the N-terminal sequence of DGD1 (NDGD1) is required for galactolipid transfer between the envelopes. Different diglycosyllipid synthases (DGD1, DGD2, and Chloroflexus glucosyltransferase) were introduced into the dgd1-1 mutant of Arabidopsis in fusion with N-terminal extensions (NDGD1 and NDGD2) targeting to the outer envelope. Reconstruction of DGDG synthesis in the outer envelope membrane was observed only with diglycosyllipid synthase fusion proteins carrying NDGD1, indicating that NDGD1 enables galactolipid translocation between envelopes. NDGD1 binds to phosphatidic acid (PA) in membranes and mediates PA-dependent membrane fusion in vitro. These findings provide a mechanism for the sorting and selective channeling of lipid precursors between the galactolipid pools of the two envelope membranes.galactolipid | chloroplast | envelope | lipid transfer T he two galactolipids, monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), are most abundant in land plants, green algae, and cyanobacteria (1). MGDG and DGDG are predominant in thylakoid membranes of chloroplasts, where they are integral components of photosystems I and II and of the light-harvesting complex II (2-4), and are essential for photosynthesis and growth (5, 6). Galactolipids are synthesized in the envelope membranes of chloroplasts (7). In tobacco and Arabidopsis, the MGDG synthase MGD1 localizes to the inner envelope where it produces the major proportion of MGDG (8, 9). The outer chloroplast envelope of Arabidopsis harbors two DGDG synthases, DGD1 and DGD2 (10, 11). DGD1 synthesizes the predominant proportion of DGDG, whereas DGD2 is active during growth under phosphate limitation. Phosphate deprivation results in the accumulation of glycolipids, including DGDG, at the expense of phospholipids and the redirection of phosphate to other cellular processes (12). DGDG synthesized by DGD1 and DGD2 is transported to thylakoid and extraplastidial membranes, respectively (11,12).Transport processes are required to channel lipid molecules between organelles and across and between different membranes (13). An ATP-binding cassette (ABC) transporter composed of three different subunits [trigalactosyldiacylglycerol1 (TGD1), -2 (TGD2), and -3 (TGD3)] is involved in the transfer of lipid precursors from the endoplasmic reticulum (ER) to the chloroplast where they are used for galactolipid synthesis. Galactolipid molecules derived from imported precursors can be distinguished from galactolipids directly synthesized in the chloroplast by the acyl composition at the sn2 position of the glycerol, with molecules containing sn2-16C acyl groups being chloroplast-derived (prokaryotic...

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Evolution of galactoglycerolipid biosynthetic pathways – From cyanobacteria to primary plastids and from primary to secondary plastids

Cited by 126 publications

References 140 publications

Light Remodels Lipid Biosynthesis in Nannochloropsis gaditana by Modulating Carbon Partitioning between Organelles

Light Remodels Lipid Biosynthesis in Nannochloropsis gaditana by Modulating Carbon Partitioning between Organelles

Configuration of the sugar head of glycolipids in thylakoid membranes

Synthesis and transfer of galactolipids in the chloroplast envelope membranes of Arabidopsis thaliana

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