Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the ‘16:3’ plant <i>Arabidopsis thaliana</i>

Browse, John; Warwick, Nigel W. M.; Somerville, Chris; Slack, C. R.

doi:10.1042/bj2350025

Cited by 343 publications

(325 citation statements)

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“…Galactolipids in algae and plants, which are comprised of C 18 and C 20 carbon fatty acids in the sn-2 position are known to have modifications which are made in the endoplasmic reticulum (ER) (Browse et al, 1986). These modifications are made by extraplastidial desaturases and elongases.…”

Section: Annotation Of Genes Involved In Galactolipid Synthesis In Cmentioning

confidence: 99%

Mono- and digalactosyldiacylglycerol composition of dinoflagellates. VI. Biochemical and genomic comparison of galactolipid biosynthesis betweenChromera velia(Chromerida), a photosynthetic alveolate with red algal plastid ancestry, and the dinoflagellate,Lingulodinium polyedrum

Dahmen

Khadka

Dodson

et al. 2013

European Journal of Phycology

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Chromera velia is a recently discovered, photosynthetic, free-living alveolate that is the closest free-living relative to nonphotosynthetic apicomplexan parasites. Most plastids, regardless of their origin, have membranes composed chiefly of two galactolipids, mono-and digalactosyldiacylglycerol (MGDG and DGDG, respectively). Because of the hypothesized shared red algal origin between the plastids of C. velia and dinoflagellates, our primary objectives were to examine how growth temperature affects MGDG and DGDG composition via positive-ion electrospray/mass spectrometry (ESI/MS) and positive ion/electrospray/ mass spectrometry/mass spectrometry (ESI/MS/MS), and to examine galactolipid biosynthetic genes to determine if shared ancestry translates into shared MGDG and DGDG composition. When growing at 20°C, C. velia produces eicosapentaenoic acidrich 20:5(n-3)/20:5(n-3) (sn-1/sn-2) MGDG and 20:5(n-3)/20:5(n-3) DGDG as its primary galactolipids, with relative percentage compositions of approximately 35 and 60%, respectively. At 30°C these are lessened by approximately 5 and 8%, respectively, by the corresponding production of 20:5/20:4 forms of these lipids. The presence of 20:5 at the sn-1 position is similar to what has been observed previously in a cluster of peridinin-containing dinoflagellates, but the presence of 20:5(n-3) at the sn-2 position is extremely rare. Thus, the forms of MGDG and DGDG in C. velia displayed similarities and differences to what has been observed in peridinin-containing dinoflagellates, such as Lingulodinium polyedrum, which produces 20:5/18:5 and 20:5/18:4 as the major forms of MGDG and DGDG. We develop conceptual models from the galactolipids observed and galactolipid-relevant gene annotations to explain the presence of polyunsaturated fatty acid-containing MGDG and DGDG in both L. polyedrum and C. velia.

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Section: Annotation Of Genes Involved In Galactolipid Synthesis In Cmentioning

confidence: 99%

Mono- and digalactosyldiacylglycerol composition of dinoflagellates. VI. Biochemical and genomic comparison of galactolipid biosynthesis betweenChromera velia(Chromerida), a photosynthetic alveolate with red algal plastid ancestry, and the dinoflagellate,Lingulodinium polyedrum

Dahmen

Khadka

Dodson

et al. 2013

European Journal of Phycology

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“…Bars denote SEs. extensively diluted by the synthesis of eukaryotic C 18 C 18 species from PC (Browse et al, 1986). PG synthesis is primarily by the prokaryotic pathway (Browse and Somerville, 1991), and the high level of labeled C 16 fatty acids incorporated into this phospholipid initially (55%) reflect the occurrence of 16:0 and 16:1(3-trans) in this lipid at the sn-2 position.…”

Section: Analysis Of Labeled Polar Lipid Classes In Wild-type and Fatmentioning

confidence: 99%

Metabolic Responses to the Reduction in Palmitate Caused by Disruption of the FATB Gene in Arabidopsis

et al. 2004

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Disruption of the FATB gene in Arabidopsis results in a two-thirds reduction in saturated fatty acids, largely palmitate, in the leaf extra-plastidic phospholipids and a reduction in the growth rate of the mutant compared to wild type (Bonaventure G, Salas JJ, Pollard MR, Ohlrogge JB [2003] Plant Cell 15: 1020-1033. In this study, we report that although fatb-ko seedlings grow more slowly than wild type, the rate of fatty acid synthesis in leaves of the mutant increases by 40%. This results in approximately the same amount of palmitate exported from the plastid as in wild type but an increase in oleate export of about 55%. To maintain constant amounts of fatty acids in leaves, thereby counterbalancing their higher rate of production, the mutant also increases its rate of fatty acid degradation. Although fatb-ko leaves have higher rates of fatty acid synthesis and turnover, the relative proportions of membrane lipids are similar to wild type. Thus, homeostatic mechanisms to preserve membrane compositions compensate for substantial changes in rates of fatty acid and glycerolipid metabolism in the mutant. Pulse-chase labeling studies show that in fatb-ko leaves there is a net increase in the synthesis of both prokaryotic and eukaryotic lipids and consequently of their turnover. The net loss of palmitate from phosphatidylcholine plus phosphatidylethanolamine is similar for wild type and mutant, suggesting that mechanisms are not present that can preferentially preserve the saturated fatty acids. In summary, the leaf cell responds to the loss of saturated fatty acid production in the fatb-ko mutant by increasing both fatty acid synthesis and degradation, but in doing so the mechanisms for increased fatty acid turnover contribute to the lowering of the percentage of saturated fatty acids found in eukaryotic lipids.In plants, the major site for de novo fatty acid synthesis (FAS) occurs in the plastid (Ohlrogge et al., 1979). Fatty acids are either utilized in this organelle or exported to supply diverse cytoplasmic biosynthetic pathways and cellular processes. Production of fatty acids for export depends on the activity of acyl-ACP thioesterases (FATs) that hydrolyze acyl-acyl carrier protein (acyl-ACP) to release free fatty acids and ACP (for review, see Voelker et al., 1997). After export, the free fatty acids are re-esterified to CoA to form the cytosolic acyl-CoA pool (Pollard and Ohlrogge, 1999). In mesophyll cells, acyl-CoAs are primarily used for the biosynthesis of membrane glycerolipids in the endoplasmic reticulum (Browse and Somerville, 1991). However, in other cell types exported fatty acids have different fates. For example, in embryo cells of oilseeds, the major fraction is incorporated into triacylglycerols, while in epidermal cells a large fraction is utilized for the synthesis of waxes and cutin (Post-Beittenmiller, 1996;Kolattukudy, 2003). Furthermore, all cells synthesize sphingolipids (Lynch, 1993), and we recently estimated that as much as 30% to 40% of exported palmitate is needed for sphingoid ba...

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“…The eukaryotic pathway involves export of 16:O and 18:l fatty acids from the chloroplast to the endoplasmic reticulum and their incorporation into phosphatidylchsline and other phospholipids that are the principal structural lipids of a0 the membranes of the cell except for the chloroplast. In addition, the diacylglycerol moiety of phosphatidylcholine can be returned to the chloroplast envelope and used as a second source af precursors for the synthesis of chloroplast glycerolipids (Browse et al, 1986b).…”

Section: Introductionmentioning

confidence: 99%

The Critical Requirement for Linolenic Acid Is Pollen Development, Not Photosynthesis, in an Arabidopsis Mutant.

1996

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The very high proportlons of trlenolc fatty acids found in chloroplast membranes of all higher plants suggest that these llpld otructurtis mlght be essentlal for photosynthasis. We report here on the productisn of Arabidopsis triple mutants that contaln negllglble levels of trlenolc fatty acids. Photosynthesls at 22OC was barely affected, and vegetative growth of the mutants was ldentlcal wlth that of tha wlld type, dm"StratIng that any requlrement for trienoic acyl groups in membrane structure and functlon 1s relatively subtle. Although vegetative growth and development were unaffected, the triple mutants are male sterlle and produce no seed under normal conditlons. Comparisons of psllen development In wlld-type and triple mutant flowersestablished that pallan gralns in the mutant develeped to the tslcellular stege. Exogenous applicatlens of a-llnolenata or jasmonate restered fertlllty. T a k n tsgether, the results demonstrate that the critical role of trlenolc acids ln tha llfe cycle of plants 1s as the precursor of sxylipln, a signallng compound that regulates final maturatlon processes and the release of pollen. INTRODUCTIONThe biophysical reactions of light harvesting and electron transport during photosynthesis take place in a uniquely constructed bilayer membrane, the thylakoid. In all photosynthetic eukaryotes, the complement of atypical glyceralipid molecules that form the foundation of this membrane are characterized by sugar headgroups and avery high leve1 of unsaturation in the fatty acid chains, which compose the central portion of the thylakoid lamella bilayer. For example, menogalactosyldiacylglycerol, the major thylakoid lipid, typically contains >90% af a-linolenic acid (183) er a combination of 183 and hexadecatrienoic (163) acids, depending on the plant species (Jamieson and Reid, 1971). These very high levels of trienoic fatty asids are noteworthy because free radicals that are byproducts of the photosynthetic llght reactions stimulate oxidation of polyunsaturated fatty acids. Because this oxidation might be expected ta medlate against a high degree of unsaturation, it has been inferred that there is a strong selective advantage to having such high levels of trienoic fatty acids in the thylakoid. Therefore, it could be reasoned that these lipid structures must have some critical role in maintaining photosynthetic functlon.To test this line of reasoning directly, we set out to develop Arabldopsis llnes with reduced levels of 18:3 and 163 fatty acids. There are two dlstinct pathways in plant 6811s for the biosynthesis of glycerolipids Rnd the associated praduction To whom correspondence should be addressed. of polyunsaturated fatty acids (Roughan et al., 1980;Browse and Somerville, 1991). 60th pathways are initiated by the synthesis of 16:O-acyl carrier protein (ACP) and 18:l-ACP by the combined action of a type II fatty acid synthase (Shimakata and Stumpf, 1982) and a soluble stearoyl-ACP desaturase (McKeon and Stumpf, 1982;Shanklin and Somerville, 1991) located in the chloroplasts or other p...

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Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the ‘16:3’ plant Arabidopsis thaliana

Cited by 343 publications

References 35 publications

Mono- and digalactosyldiacylglycerol composition of dinoflagellates. VI. Biochemical and genomic comparison of galactolipid biosynthesis betweenChromera velia(Chromerida), a photosynthetic alveolate with red algal plastid ancestry, and the dinoflagellate,Lingulodinium polyedrum

Mono- and digalactosyldiacylglycerol composition of dinoflagellates. VI. Biochemical and genomic comparison of galactolipid biosynthesis betweenChromera velia(Chromerida), a photosynthetic alveolate with red algal plastid ancestry, and the dinoflagellate,Lingulodinium polyedrum

Metabolic Responses to the Reduction in Palmitate Caused by Disruption of the FATB Gene in Arabidopsis

The Critical Requirement for Linolenic Acid Is Pollen Development, Not Photosynthesis, in an Arabidopsis Mutant.

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