Metabolic Interactions between the Lands Cycle and the Kennedy Pathway of Glycerolipid Synthesis in <i>Arabidopsis</i> Developing Seeds

Wang, Liping; Shen, Wenyun; Kazachkov, Michael; Chen, Guanqun; Chen, Qilin; Carlsson, Anders S.; Stymne, Sten; Weselake, Randall J.; Zou, Jitao

doi:10.1105/tpc.112.104604

Cited by 144 publications

(156 citation statements)

References 78 publications

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“…However, kinetic labeling data indicate that fatty acids exported from the plastid are first incorporated into PC and then channeled to TAG in soybean embryos (Bates et al, 2009Bates and Browse, 2011). The presence of highly active LPCAT on the Arabidopsis plastid outer envelope membrane is consistent with the formation of PC using fatty acids from the plastids (Tjellström et al, 2012;Wang et al, 2012a). Recent data indicate that LPCAT1 and LPCAT2 catalyze the incorporation of fatty acids into PC in Arabidopsis seeds Wang et al, 2012a).…”

Section: Discussionmentioning

confidence: 71%

“…The presence of highly active LPCAT on the Arabidopsis plastid outer envelope membrane is consistent with the formation of PC using fatty acids from the plastids (Tjellström et al, 2012;Wang et al, 2012a). Recent data indicate that LPCAT1 and LPCAT2 catalyze the incorporation of fatty acids into PC in Arabidopsis seeds Wang et al, 2012a). However, knowledge is lacking about what enzyme produces LPC that impacts TAG synthesis.…”

Section: Discussionmentioning

confidence: 80%

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Patatin-Related Phospholipase pPLAIIIδ Increases Seed Oil Content with Long-Chain Fatty Acids in Arabidopsis

Bahn

Fan

et al. 2013

Plant Physiology

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The release of fatty acids from membrane lipids has been implicated in various metabolic and physiological processes, but in many cases, the enzymes involved and their functions in plants remain unclear. Patatin-related phospholipase As (pPLAs) constitute a major family of acyl-hydrolyzing enzymes in plants. Here, we show that pPLAIIId promotes the production of triacylglycerols with 20-and 22-carbon fatty acids in Arabidopsis (Arabidopsis thaliana). Of the four pPLAIIIs (a, b, g, d), only pPLAIIId gene knockout results in a decrease in seed oil content, and pPLAIIId is most highly expressed in developing embryos. The overexpression of pPLAIIId increases the content of triacylglycerol and 20-and 22-carbon fatty acids in seeds with a corresponding decrease in 18-carbon fatty acids. Several genes in the glycerolipid biosynthetic pathways are up-regulated in pPLAIIId-overexpressing siliques. pPLAIIId hydrolyzes phosphatidylcholine and also acyl-coenzyme A to release fatty acids. pPLAIIId-overexpressing plants have a lower level, whereas pPLAIIId knockout plants have a higher level, of acyl-coenzyme A than the wild type. Whereas seed yield decreases in transgenic plants that ubiquitously overexpress pPLAIIId, seed-specific overexpression of pPLAIIId increases seed oil content without any detrimental effect on overall seed yield. These results indicate that pPLAIIId-mediated phospholipid turnover plays a role in fatty acid remodeling and glycerolipid production.Lipids play essential structural, metabolic, and regulatory roles in plant growth, development, and stress responses. In addition, plant lipids are a major source of food and renewable materials for various industrial and energy applications (Dyer et al., 2008;Hayden

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Section: Discussionmentioning

confidence: 71%

Section: Discussionmentioning

confidence: 80%

Patatin-Related Phospholipase pPLAIIIδ Increases Seed Oil Content with Long-Chain Fatty Acids in Arabidopsis

Bahn

Fan

et al. 2013

Plant Physiology

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“…Acyl turnover in membrane lipids, through a cycle of deacylation/ acylation of PC to lysophosphatidylcholine (LPC), was first described by Lands (1958). Substantial progress has been made in the understanding of the acylation mechanism of LPC, involving lysophosphatidylcholine acyltransferases (LPCAT; Ståhl et al, 2008;Wang et al, 2012;Xu et al, 2012). As suggested by Lands (1960), PC deacylation was initially thought to result from the activity of a phospholipase.…”

mentioning

confidence: 99%

“…With recent developments in the understanding of lipid biosynthesis, focusing on FA incorporation and turnover in phosphatidylcholine (PC), attention is moving from the traditional Kennedy pathway of lipid synthesis to that of acyl editing Wang et al, 2012;Xu et al, 2012), with the relative importance of each pathway in lipid synthesis depending on the plant species . Acyl turnover in membrane lipids, through a cycle of deacylation/ acylation of PC to lysophosphatidylcholine (LPC), was first described by Lands (1958).…”

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confidence: 99%

A Small Phospholipase A2-α from Castor Catalyzes the Removal of Hydroxy Fatty Acids from Phosphatidylcholine in Transgenic Arabidopsis Seeds

et al. 2015

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Ricinoleic acid, an industrially useful hydroxy fatty acid (HFA), only accumulates to high levels in the triacylglycerol fraction of castor (Ricinus communis) endosperm, even though it is synthesized on the membrane lipid phosphatidylcholine (PC) from an oleoyl ester. The acyl chains of PC undergo intense remodeling through the process of acyl editing. The identities of the proteins involved in this process, however, are unknown. A phospholipase A2 (PLA2) is thought to be involved in the acyl-editing process. We show here a role for RcsPLA2α in the acyl editing of HFA esterified to PC. RcsPLA2α was identified by its high relative expression in the castor endosperm transcriptome. Coexpression in Arabidopsis (Arabidopsis thaliana) seeds of RcsPLA2α with the castor fatty acid hydroxylase RcFAH12 led to a dramatic decrease in seed HFA content when compared with RcFAH12 expression alone in both PC and the neutral lipid fraction. The low-HFA trait was heritable and gene dosage dependent, with hemizygous lines showing intermediate HFA levels. The low seed HFA levels suggested that RcsPLA2α functions in vivo as a PLA2 with HFA specificity. Activity assays with yeast (Saccharomyces cerevisiae) microsomes showed a high specificity of RcsPLA2α for ricinoleic acid, superior to that of the endogenous Arabidopsis PLA2α. These results point to RcsPLA2α as a phospholipase involved in acyl editing, adapted to specifically removing HFA from membrane lipids in seeds.

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“…For example, PC can be produced through esterification of FA to lysophosphatidylcholine (LPC) with lysophosphatidylcholine acyltransferase (LPCAT; Stymne and Stobart, 1984;Bates et al, 2012;Wang et al, 2012) and after modification the FA is released for reentry into the acyl-CoA pool, regenerating LPC and completing the cycle in a process coined acyl editing (Williams et al, 2000;Bates et al, 2009;Bates and Browse, 2012;Tjellström et al, 2012). In soybean (Glycine max) and Arabidopsis it is estimated that .90% of nascent FAs flux through PC by acyl editing or as DAG components before incorporation into TAG (Bates et al, 2009;Browse, 2011, 2012).…”

mentioning

confidence: 99%

Phospholipase Dζ Enhances Diacylglycerol Flux into Triacylglycerol

Yang

Wang

et al. 2017

Plant Physiol.

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Plant seeds are the primary source of triacylglycerols (TAG) for food, feed, fuel, and industrial applications. As TAG is produced from diacylglycerol (DAG), successful engineering strategies to enhance TAG levels have focused on the conversion of DAG to TAG. However, the production of TAG can be limited by flux through the enzymatic reactions that supply DAG. In this study, two Arabidopsis phospholipase D z genes (AtPLD z1 and AtPLD z2 ) were coexpressed in Camelina sativa to test whether the conversion of phosphatidylcholine to DAG impacts TAG levels in seeds. The resulting transgenic plants produced 2% to 3% more TAG as a component of total seed biomass and had increased 18:3 and 20:1 fatty acid levels relative to wild type. Increased DAG and decreased PC levels were examined through the kinetics of lipid assembly by [ 14 C]acetate and [ 14 C]glycerol incorporation into glycerolipids. [ 14 C]acetate was rapidly incorporated into TAG in both wild-type and overexpression lines, indicating a significant flux of nascent and elongated acyl-CoAs into the sn-3 position of TAG. Stereochemical analysis revealed that newly synthesized fatty acids were preferentially incorporated into the sn-2 position of PC, but the sn-1 position of de novo DAG and indicated similar rates of nascent acyl groups into the Kennedy pathway and acyl editing. [ 14 C]glycerol studies demonstrated PC-derived DAG is the major source of DAG for TAG synthesis in both tissues. The results emphasize that the interconversions of DAG and PC pools can impact oil production and composition.

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Metabolic Interactions between the Lands Cycle and the Kennedy Pathway of Glycerolipid Synthesis in Arabidopsis Developing Seeds

Cited by 144 publications

References 78 publications

Patatin-Related Phospholipase pPLAIIIδ Increases Seed Oil Content with Long-Chain Fatty Acids in Arabidopsis

Patatin-Related Phospholipase pPLAIIIδ Increases Seed Oil Content with Long-Chain Fatty Acids in Arabidopsis

A Small Phospholipase A2-α from Castor Catalyzes the Removal of Hydroxy Fatty Acids from Phosphatidylcholine in Transgenic Arabidopsis Seeds

Phospholipase Dζ Enhances Diacylglycerol Flux into Triacylglycerol

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