Compartmentation of Triacylglycerol Accumulation in Plants

Abstract

Triacylglycerols from plants, familiar to most people as vegetable oils, supply 25% of dietary calories to the developed world and are increasingly a source for renewable biomaterials and fuels. Demand for vegetable oils will double by 2030, which can be met only by increased oil production. Triacylglycerol synthesis is accomplished through the coordinate action of multiple pathways in multiple subcellular compartments. Recent information has revealed an underappreciated complexity in pathways for synthesis and accumulation of this important energyrich class of molecules. Regulation of Fatty Acid Supply by PlastidsPlant fatty acid (FA) 2 synthesis differs from almost all other eukaryotes in two fundamental features. First, unlike the cytosolic location in other kingdoms, FAs for triacylglycerol (TAG) and membrane synthesis are produced in the plastid compartment of plant cells: chloroplasts in green tissues and proplastids (or leucoplasts) in non-green tissues. Second, the plant FA synthase (FAS) is a dissociable complex with separate proteins for the acyl carrier protein (ACP) and each enzyme (1). After assembly of C 16 and C 18 acyl chains by FAS and desaturation of C 18:0 to C 18:1 , FAs destined for TAG assembly are released from ACP in the plastid stroma by chain-terminating acyl-ACP thioesterases. Two classes of thioesterases designated FATA and FATB are responsible for hydrolysis of unsaturated and saturated acyl-ACPs, respectively, and thus determine in large part the chain length and saturated FA content of plant oils (2). The FA products of FATA and FATB are activated to CoA before export to the endoplasmic reticulum (ER). The subsequent reactions of TAG synthesis belong to the so-called "eukaryotic" pathway of glycerolipid synthesis, which occurs outside the plastid (3, 4). An overview of the compartmentalization of FA supply for TAG is shown in Fig. 1. FA production by plastids can limit TAG accumulation in seeds (5, 6), so increasing flux through FA biosynthesis may perhaps have the single greatest influence on the amount of TAG produced in plant tissues. As in bacteria, fungi, and animals, both in vitro and in vivo evidence indicates that acetylCoA carboxylase (ACCase) is a key rate-determining step that controls FA biosynthesis. ACCase activity is under complex regulation by light, phosphorylation, thioredoxin, PII protein, and product feedback control (7,8). Of course, the flux of carbon to FA synthesis can have multiple regulatory steps, which may explain why efforts to increase seed oil by up-regulating ACCase were only modestly successful (9).Transcriptional regulation of the production of FA for TAG biosynthesis is most directly controlled by the WRINKLED1 transcription factor (7, 10, 11). Arabidopsis wri1 mutants are reduced by 80% in seed oil, and overexpression of WRI1 can increase oil content in seeds of several plants. Targets of WRI1 include ACCase, many enzymes of FAS, and key enzymes and transporters that provide pyruvate and acetyl-CoA in the plastid. Thus, WRI1 can be considered as ...

Methylcrotonyl-CoA Carboxylase Regulates Triacylglycerol Accumulation in the Model Diatom Phaeodactylum tricornutum

“…Although it was postulated that catabolism of amino acids in microalgae under nitrogen starvation would yield various TCA intermediates that could feed into the TCA cycle and be directed to fatty acid biosynthesis (Hockin et al, 2012;Radakovits et al, 2012), our findings provide compelling evidence that it is principally BCAA catabolism that contributes to TAG biosynthesis in this way. Responses of genes encoding lipid biosynthetic enzymes during TAG accumulation in P. tricornutum were almost the same as those in plants and C. reinhardtii (Miller et al, 2010;Chapman and Ohlrogge, 2012), but different from those in oleaginous Nannochloropsis species (Radakovits et al, 2012;Vieler et al, 2012). Nannochloropsis species constitutively produce TAG even during logarithmic growth, and few genes that are directly involved in lipid biosynthesis are transcriptionally upregulated to a significant extent.…”

Choreography of Transcriptomes and Lipidomes ofNannochloropsisReveals the Mechanisms of Oil Synthesis in Microalgae

“…Enzymes of the Kennedy pathway are often encoded by multiple copies of genes or are distinct proteins in eukaryotes (Coleman and Lee, 2004). In some cases in vascular plants, isoforms of the enzymes are associated with different subcellular compartments and involved in diverse physiological functions (Chapman and Ohlrogge, 2012). Thus, identifying the genes specifically underlying TAG synthesis is essential for understanding lipid metabolism and for overproducing lipids of commercial interest in microalgae.…”

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

“…To date, although most of the enzymatic steps in lipid biosynthesis are defined at the moleculargenetic level in several model organisms (Nohturfft and Zhang, 2009;Chapman and Ohlrogge, 2012;Henry et al, 2012), the signals and mechanisms regulating intracellular lipid homeostasis are less well defined (Nohturfft and Zhang, 2009;Hermansson et al, 2011, Holthuis andMenon, 2014), particularly in plants (Bonaventure et al, 2004;Kunz et al, 2009;Zhang et al, 2009;Fan et al, 2013a;Park et al, 2013).…”