Arabidopsis Mutants in Short- and Medium-chain Acyl-CoA Oxidase Activities Accumulate Acyl-CoAs and Reveal That Fatty Acid β-Oxidation Is Essential for Embryo Development

Rylott, Elizabeth L.; Rogers, Caroline A.; Gilday, Alison D.; Edgell, Teresa; Larson, Tony R.; Graham, Ian A.

doi:10.1074/jbc.m300826200

Cited by 102 publications

(119 citation statements)

References 51 publications

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“…Similar phenotypes are found in the ped1ped3 double mutant, where acyl-CoA import and its subsequent cleavage in peroxisomes are both impaired (Hayashi et al, 2002). Moreover, combination of loss-of-function mutations in the peroxisomal medium-and short-chain acyl-CoA oxidase genes leads to early embryo lethality (Rylott et al, 2003). These phenomena suggest that peroxisomal b-oxidation is essential for normal tissue and organ growth throughout the plant life cycle, but the underlying molecular basis remains elusive.…”

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confidence: 48%

The Peroxisome Deficient Arabidopsis Mutant sse1 Exhibits Impaired Fatty Acid Synthesis

2004

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The Arabidopsis Shrunken Seed 1 (SSE1) gene encodes a homolog of the peroxisome biogenesis factor Pex16p, and a loss-of-function mutation in this gene alters seed storage composition. Two lines of evidence support a function for SSE1 in peroxisome biogenesis: the peroxisomal localization of a green fluorescent protein-SSE1 fusion protein and the lack of normal peroxisomes in sse1 mutant embryos. The green fluorescent protein-SSE1 colocalizes with the red fluorescent protein (RFP)-labeled peroxisomal markers RFP-peroxisome targeting signal 1 and peroxisome targeting signal 2-RFP in transgenic Arabidopsis. Each peroxisomal marker exhibits a normal punctate peroxisomal distribution in the wild type but not the sse1 mutant embryos. Further studies reported here were designed toward understanding carbon metabolism in the sse1 mutant. A time course study of dissected embryos revealed a dramatic rate decrease in oil accumulation and an increase in starch accumulation. Introduction of starch synthesis mutations into the sse1 background did not restore oil biosynthesis. This finding demonstrated that reduction in oil content in sse1 is not caused by increased carbon flow to starch. To identify the blocked steps in the sse1 oil deposition pathway, developing sse1 seeds were supplied radiolabeled oil synthesis precursors. The ability of sse1 to incorporate oleic acid, but not pyruvate or acetate, into triacylglycerol indicated a defect in the fatty acid biosynthetic pathway in this mutant. Taken together, the results point to a possible role for peroxisomes in the net synthesis of fatty acids in addition to their established function in lipid catabolism. Other possible interpretations of the results are discussed.

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confidence: 48%

The Peroxisome Deficient Arabidopsis Mutant sse1 Exhibits Impaired Fatty Acid Synthesis

2004

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“…The molecular identity of the core b-oxidation pathway components and their physiological role in FA catabolism in postgerminative seedling growth in oilseeds are now well established (Graham, 2008;Theodoulou and Eastmond, 2012). Physiological understanding of b-oxidation in mature plant tissues has been defined in dark-induced (Kunz et al, 2009) or natural (Yang and Ohlrogge, 2009) senescence, reproductive development (Rylott et al, 2003;Footitt et al, 2007aFootitt et al, , 2007b, with respect to the biosynthesis of auxin (Strader and Bartel, 2011) and jasmonate (Goepfert and Poirier, 2007), and during storage TAG production (Slocombe et al, 2009;Kelly et al, 2013). The results of this study provide new insights into the regulation of the peroxisomal b-oxidation pathway and its role in membrane lipid homeostasis in leaves.…”

Section: Discussionmentioning

confidence: 99%

Arabidopsis Lipins, PDAT1 Acyltransferase, and SDP1 Triacylglycerol Lipase Synergistically Direct Fatty Acids toward β-Oxidation, Thereby Maintaining Membrane Lipid Homeostasis

et al. 2014

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Triacylglycerol (TAG) metabolism is a key aspect of intracellular lipid homeostasis in yeast and mammals, but its role in vegetative tissues of plants remains poorly defined. We previously reported that PHOSPHOLIPID:DIACYLGLYCEROL ACYLTRANSFERASE1 (PDAT1) is crucial for diverting fatty acids (FAs) from membrane lipid synthesis to TAG and thereby protecting against FA-induced cell death in leaves. Here, we show that overexpression of PDAT1 enhances the turnover of FAs in leaf lipids. Using the trigalactosyldiacylglycerol1-1 (tgd1-1) mutant, which displays substantially enhanced PDAT1-mediated TAG synthesis, we demonstrate that disruption of SUGAR-DEPENDENT1 (SDP1) TAG lipase or PEROXISOMAL TRANSPORTER1 (PXA1) severely decreases FA turnover, leading to increases in leaf TAG accumulation, to 9% of dry weight, and in total leaf lipid, by 3-fold. The membrane lipid composition of tgd1-1 sdp1-4 and tgd1-1 pxa1-2 double mutants is altered, and their growth and development are compromised. We also show that two Arabidopsis thaliana lipin homologs provide most of the diacylglycerol for TAG synthesis and that loss of their functions markedly reduces TAG content, but with only minor impact on eukaryotic galactolipid synthesis. Collectively, these results show that Arabidopsis lipins, along with PDAT1 and SDP1, function synergistically in directing FAs toward peroxisomal b-oxidation via TAG intermediates, thereby maintaining membrane lipid homeostasis in leaves.

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“…The abnormal inflorescence meristem1 (aim1) mutation, which eliminates one of the two multifunctional proteins (MFP), indicates the importance of b-oxidation during floral development (Richmond and Bleecker, 1999). A double mutant in which two members of the acyl-CoA oxidase (ACX) gene family are mutated (acx3 and acx4) is embryo lethal, showing that b-oxidation is essential for seed development as well as germination (Rylott et al, 2003). Thus, it is clear from studies in which fatty acid b-oxidation is blocked that distinct phenotypes are obtained.…”

Section: Introductionmentioning

confidence: 99%

Arabidopsis Peroxisomal Citrate Synthase Is Required for Fatty Acid Respiration and Seed Germination

2005

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We tested the hypothesis that peroxisomal citrate synthase (CSY) is required for carbon transfer from peroxisomes to mitochondria during respiration of triacylglycerol in Arabidopsis thaliana seedlings. Two genes encoding peroxisomal CSY are expressed in Arabidopsis seedlings, and seeds from plants with both CSY genes disrupted were dormant and did not metabolize triacylglycerol. Germination was achieved by removing the seed coat and supplying sucrose, but the seedlings still did not use triacylglycerol. The mutant seedlings were resistant to 2,4-dichlorophenoxybutyric acid, indicating a block in peroxisomal b-oxidation, and were unable to develop further after transfer to soil. The mutant phenotype was complemented with a cDNA encoding CSY with either its native peroxisomal targeting sequence (PTS2) or a heterologous PTS1 sequence from pumpkin (Cucurbita pepo) malate synthase. These results suggest that peroxisomal CSY in Arabidopsis is not only a key enzyme of the glyoxylate cycle but also catalyzes an essential step in the respiration of fatty acids. We conclude that citrate is exported from the peroxisome during fatty acid respiration, whereas in yeast, acetylcarnitine is exported.

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Arabidopsis Mutants in Short- and Medium-chain Acyl-CoA Oxidase Activities Accumulate Acyl-CoAs and Reveal That Fatty Acid β-Oxidation Is Essential for Embryo Development

Cited by 102 publications

References 51 publications

The Peroxisome Deficient Arabidopsis Mutant sse1 Exhibits Impaired Fatty Acid Synthesis

The Peroxisome Deficient Arabidopsis Mutant sse1 Exhibits Impaired Fatty Acid Synthesis

Arabidopsis Lipins, PDAT1 Acyltransferase, and SDP1 Triacylglycerol Lipase Synergistically Direct Fatty Acids toward β-Oxidation, Thereby Maintaining Membrane Lipid Homeostasis

Arabidopsis Peroxisomal Citrate Synthase Is Required for Fatty Acid Respiration and Seed Germination

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