Tracking synthesis and turnover of triacylglycerol in leaves

Tjellström, Henrik; Strawsine, Merissa; Ohlrogge, John B.

doi:10.1093/jxb/eru500

Cited by 52 publications

(37 citation statements)

References 73 publications

(104 reference statements)

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“…In the latter case, the DGAT1 gene exhibited increased expression levels in ambient air, and this was reversed by the 1% CO 2 treatment. This finding reflects the importance of DGAT1 as a major regulator of the TAG biosynthetic pathway in seedling plants, as evidenced by the previous analysis of dgat1 mutants, which display a major reduction in leaf TAG accumulation (Zhang et al, 2009;Tjellström et al, 2015).…”

Section: Mthd Contributes To Photorespirationsupporting

confidence: 79%

Discovery and Characterization of the 3-Hydroxyacyl-ACP Dehydratase Component of the Plant Mitochondrial Fatty Acid Synthase System

et al. 2017

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We report the characterization of the Arabidopsis (Arabidopsis thaliana) 3-hydroxyacyl-acyl carrier protein dehydratase (mtHD) component of the mitochondrial fatty acid synthase (mtFAS) system, encoded by AT5G60335. The mitochondrial localization and catalytic capability of mtHD were demonstrated with a green fluorescent protein transgenesis experiment and by in vivo complementation and in vitro enzymatic assays. RNA interference (RNAi) knockdown lines with reduced mtHD expression exhibit traits typically associated with mtFAS mutants, namely a miniaturized morphological appearance, reduced lipoylation of lipoylated proteins, and altered metabolomes consistent with the reduced catalytic activity of lipoylated enzymes. These alterations are reversed when mthd-rnai mutant plants are grown in a 1% CO 2 atmosphere, indicating the link between mtFAS and photorespiratory deficiency due to the reduced lipoylation of glycine decarboxylase. In vivo biochemical feeding experiments illustrate that sucrose and glycolate are the metabolic modulators that mediate the alterations in morphology and lipid accumulation. In addition, both mthd-rnai and mtkas mutants exhibit reduced accumulation of 3-hydroxytetradecanoic acid (i.e. a hallmark of lipid A-like molecules) and abnormal chloroplastic starch granules; these changes are not reversible by the 1% CO 2 atmosphere, demonstrating two novel mtFAS functions that are independent of photorespiration. Finally, RNA sequencing analysis revealed that mthd-rnai and mtkas mutants are nearly equivalent to each other in altering the transcriptome, and these analyses further identified genes whose expression is affected by a functional mtFAS system but independent of photorespiratory deficiency. These data demonstrate the nonredundant nature of the mtFAS system, which contributes unique lipid components needed to support plant cell structure and metabolism.

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Section: Mthd Contributes To Photorespirationsupporting

confidence: 79%

Discovery and Characterization of the 3-Hydroxyacyl-ACP Dehydratase Component of the Plant Mitochondrial Fatty Acid Synthase System

et al. 2017

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“…In addition, extensive experimental evidence indicates that free FAs supplied to tissues are sequestered into TAGs (Roughan et al, 1987;Koo et al, 2005;Tjellström et al, 2015). These TAGs undergo substantial and rapid turnover (Tjellström et al, 2015).…”

Section: Tag Turnover Is Increased In Vegetative Tissues Of B Distacmentioning

confidence: 99%

“…These TAGs undergo substantial and rapid turnover (Tjellström et al, 2015). Moreover, the expression of many orthologs presumed to encode enzymes involved in TAG degradation was induced, suggesting that this pathway is highly active (Fig.…”

Section: Tag Turnover Is Increased In Vegetative Tissues Of B Distacmentioning

confidence: 99%

Ectopic expression of WRI1 affects fatty acid homeostasis in Brachypodium distachyon vegetative tissues

et al. 2015

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Triacylglycerol (TAG) is a storage lipid used for food purposes and as a renewable feedstock for biodiesel production. WRINKLED1 (WRI1) is a transcription factor that governs fatty acid (FA) synthesis and, indirectly, TAG accumulation in oil-storing plant tissues, and its ectopic expression has led to TAG accumulation in vegetative tissues of different dicotyledonous plants. The ectopic expression of BdWRI1 in the grass Brachypodium distachyon induced the transcription of predicted genes involved in glycolysis and FA biosynthesis, and TAG content was increased up to 32.5-fold in 8-week-old leaf blades. However, the ectopic expression of BdWRI1 also caused cell death in leaves, which has not been observed previously in dicotyledonous plants such as Arabidopsis (Arabidopsis thaliana). Lipid analysis indicated that the free FA content was 2-fold elevated in BdWRI1-expressing leaf blades of B. distachyon. The transcription of predicted genes involved in b-oxidation was induced. In addition, linoleic FA treatment caused cell death in B. distachyon leaf blades, an effect that was reversed by the addition of the FA biosynthesis inhibitor cerulenin. Taken together, ectopic expression of BdWRI1 in B. distachyon enhances FA biosynthesis and TAG accumulation in leaves, as expected, but also leads to increased free FA content, which has cytotoxic effects leading to cell death. Thus, while WRI appears to ubiquitously affect FA biosynthesis and TAG accumulation in diverse plants, its ectopic expression can lead to undesired side effects depending on the context of the specific lipid metabolism of the respective plant species.

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“…The presence of high biochemical activities for TAG synthesis (Dahlqvist et al, 2000) and breakdown (Tjellström et al, 2015) raises an intriguing question of the functional role for TAG metabolism in plant vegetative tissues. Early studies in yeast and mammals showed that TAG accumulation plays a pivotal role in sequestering FFAs (Listenberger et al, 2003) and DAG (Zhang et al, 2003) into lipid droplets and thereby protecting against lipotoxic cell death under cellular conditions of fatty acid overload.…”

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confidence: 99%

A Central Role for Triacylglycerol in Membrane Lipid Breakdown, Fatty Acid β-Oxidation, and Plant Survival under Extended Darkness

2017

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ORCID IDs: 0000-0002-6821-6583 (J.F.); 0000-0002-0595-081X (L.Y.); 000-0002-0179-9462 (C.X.).Neutral lipid metabolism is a key aspect of intracellular homeostasis and energy balance and plays a vital role in cell survival under adverse conditions, including nutrient deprivation in yeast and mammals, but the role of triacylglycerol (TAG) metabolism in plant stress response remains largely unknown. By thoroughly characterizing mutants defective in SUGAR-DEPENDENT1 (SDP1) triacylglycerol lipase or PEROXISOMAL ABC TRANSPORTER 1 (PXA1), here we show that TAG is a key intermediate in the mobilization of fatty acids from membrane lipids for peroxisomal b-oxidation under prolonged dark treatment. Disruption of SDP1 increased TAG accumulation in cytosolic lipid droplets and markedly enhanced plant tolerance to extended darkness. We demonstrate that blocking TAG hydrolysis enhances plant tolerance to dark treatment via two distinct mechanisms. In pxa1 mutants, in which free fatty acids accumulated rapidly under extended darkness, SDP1 disruption resulted in a marked decrease in levels of cytotoxic lipid intermediates such as free fatty acids and phosphatidic acid, suggesting a buffer function of TAG accumulation against lipotoxicity under fatty acid overload. In the wild type, in which free fatty acids remained low and unchanged under dark treatment, disruption of SDP1 caused a decrease in reactive oxygen species production and hence the level of lipid peroxidation, indicating a role of TAG in protection against oxidative damage. Overall, our findings reveal a crucial role for TAG metabolism in membrane lipid breakdown, fatty acid turnover, and plant survival under extended darkness.Photosynthesis provides the energy and reduced carbon for metabolism, growth, storage, and maintenance throughout the daily cycle. During the day, light energy is used to fuel photosynthetic carbon assimilation to produce organic compounds. In many plants including Arabidopsis (Arabidopsis thaliana), the majority of the immediate stable products of photosynthesis (up to 80%) are used for the synthesis of sugars and starch (Smith and Stitt, 2007;Stitt and Zeeman, 2012). At night when photosynthesis is not possible, starch accumulated during the day is hydrolyzed to provide a steady sugar and energy supply. A small fraction (approximately 10%) of photosynthetic carbon is used for the synthesis of fatty acids in the chloroplast in the light (Murphy and Leech, 1981). The end products of fatty acid synthesis can be used to acylate glycerol-3-phosphate (G3P) by acyltransferases to produce phosphatidic acid (PA) in the chloroplast, or in the endoplasmic reticulum (ER) following their export from the chloroplast (Bates et al., 2013). Dephosphorylation of PA yields diacylglycerol (DAG) in the ER and the chloroplast. Because the substrate specificity of enzymes responsible for PA assembly in the two compartments differs, DAG formed in the chloroplast or the ER is characterized by the presence of 16-or 18-carbon fatty acids at the sn-2 position of glycer...

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Tracking synthesis and turnover of triacylglycerol in leaves

Abstract: HighlightAnalysis of flux of exogenously supplied [14C]fatty acid in wild-type and mutant Arabidopsis leaves indicates that DGAT1 is the predominant enzyme involved in triacylglycerol synthesis in young leaves.

Cited by 52 publications

References 73 publications

Discovery and Characterization of the 3-Hydroxyacyl-ACP Dehydratase Component of the Plant Mitochondrial Fatty Acid Synthase System

Discovery and Characterization of the 3-Hydroxyacyl-ACP Dehydratase Component of the Plant Mitochondrial Fatty Acid Synthase System

Ectopic expression of WRI1 affects fatty acid homeostasis in Brachypodium distachyon vegetative tissues

A Central Role for Triacylglycerol in Membrane Lipid Breakdown, Fatty Acid β-Oxidation, and Plant Survival under Extended Darkness

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