<i>Arabidopsis</i>
            lipins mediate eukaryotic pathway of lipid metabolism and cope critically with phosphate starvation

Nakamura, Yuki; Koizumi, Ryota; Shui, Guanghou; Shimojima, Mie; Wenk, Markus R.; Ito, Toshiro; Ohta, Hiroyuki

doi:10.1073/pnas.0907173106

Cited by 244 publications

(259 citation statements)

References 45 publications

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“…Two homologous genes designated PAH1 and PAH2 have been identified in Arabidopsis (54 -56). Loss of function of PAH1 and PAH2 in Arabidopsis disrupted membrane remodeling, suggesting a role in the eukaryotic pathway of DAG formation (54). Furthermore, pah1/pah2 double mutants showed increased PC and overall expansion of the ER in leaves, consistent with a function in regulating membrane phospholipid accumulation as in animals and yeast (55), although the mechanism(s) remain to be elucidated.…”

Section: Conventional Kennedy Pathwaymentioning

confidence: 86%

Compartmentation of Triacylglycerol Accumulation in Plants

Chapman

Ohlrogge

2012

Journal of Biological Chemistry

406

352

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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 ...

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Section: Conventional Kennedy Pathwaymentioning

confidence: 86%

Compartmentation of Triacylglycerol Accumulation in Plants

Chapman

Ohlrogge

2012

Journal of Biological Chemistry

406

352

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“…To verify if altered levels of PCho and PEth could lead to the transcriptomic activation or inhibition of specific lipid metabolism pathways, we selected several genes representative of membrane lipid recycling pathways triggered during Pi starvation (Nakamura, 2013). These genes included NPC4 (representative of the nonspecific PLC pathway; Nakamura et al, 2005), PLDz1 and 2, PAH1 and 2 (for the PLD/PAP pathway; Qin and Wang, 2002;Li et al, 2006;Nakamura et al, 2009;Eastmond et al, 2010), and GDPD1, 2, 3, 5, and 6 (for the LAH/GDPD pathway; Cheng et al, 2011). In response to a lack of Pi, we observed that NPC4, PLDz2, and GDPD1, 2, 3, 5, and 6 were induced in wild-type plants as previously reported (Supplemental Fig.…”

Section: Triple Ko Mutant Does Not Mimic or Amplify Phenotypes Causedmentioning

confidence: 99%

The Phosphate Fast-Responsive Genes PECP1 and PPsPase1 Affect Phosphocholine and Phosphoethanolamine Content

et al. 2018

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Phosphate starvation-mediated induction of the HAD-type phosphatases PPsPase1 (AT1G73010) and PECP1 (AT1G17710) has been reported in Arabidopsis (Arabidopsis thaliana). However, little is known about their in vivo function or impact on plant responses to nutrient deficiency. The preferences of PPsPase1 and PECP1 for different substrates have been studied in vitro but require confirmation in planta. Here, we examined the in vivo function of both enzymes using a reverse genetics approach. We demonstrated that PPsPase1 and PECP1 affect plant phosphocholine and phosphoethanolamine content, but not the pyrophosphate-related phenotypes. These observations suggest that the enzymes play a similar role in planta related to the recycling of polar heads from membrane lipids that is triggered during phosphate starvation. Altering the expression of the genes encoding these enzymes had no effect on lipid composition, possibly due to compensation by other lipid recycling pathways triggered during phosphate starvation. Furthermore, our results indicated that PPsPase1 and PECP1 do not influence phosphate homeostasis, since the inactivation of these genes had no effect on phosphate content or on the induction of molecular markers related to phosphate starvation. A combination of transcriptomics and imaging analyses revealed that PPsPase1 and PECP1 display a highly dynamic expression pattern that closely mirrors the phosphate status. This temporal dynamism, combined with the wide range of induction levels, broad expression, and lack of a direct effect on Pi content and regulation, makes PPsPase1 and PECP1 useful molecular markers of the phosphate starvation response.Plant growth is highly sensitive to a lack of phosphate (Pi); hence, the application of Pi fertilizers has become standard practice for high-throughput crop production (Cordell et al., 2009). Most phosphorus in the soil is not available to plants, as it is combined with other minerals or parts of organic compounds (Bieleski, 1973;Raghothama and Karthikeyan, 2005). Only a small fraction of soluble Pi (usually present at a concentration of ,10 mM in the soil) can be taken up by plants.Although growth is not optimal under limiting conditions, plants can withstand changing Pi concentrations within heterogeneous soils or in the external nutrient supply that can lead to reprogramming of their metabolism and architecture (Hammond et al., 2003;Péret et al., 2011;Plaxton and Tran, 2011). Root architecture can be modified to facilitate Pi uptake by favoring the development of lateral roots (at the expense of primary root elongation in many plants including Arabidopsis), increasing the density and length of root hairs, and limiting the development of aerial parts (López-Bucio et al., 2002;Svistoonoff et al., 2007;Gruber et al., 2013). Pi uptake mechanisms are enhanced at the root/soil interface, particularly through the stimulation of Pi transport activity (Mudge et al., 2002;Shin et al., 2004;Nussaume et al., 2011; Ayadi et al., 2015). In parallel, mobilization of Pi sources fr...

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“…The Arabidopsis genome harbors two highly similar lipin homolog genes encoding Mg 2+ -dependent PAHs that function redundantly in catalyzing the dephosphorylation of phosphatidic acid (PA) to DAG (Nakamura et al, 2009;Eastmond et al, 2010), the direct precursor of TAG and phospholipids. To test their role in TAG synthesis and FA degradation in leaves, we constructed a double mutant lacking PAH1 and PAH2 by genetic crossing.…”

Section: Pah1 and Pah2 Are Required For Tag Synthesis In Leavesmentioning

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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Arabidopsis lipins mediate eukaryotic pathway of lipid metabolism and cope critically with phosphate starvation

Cited by 244 publications

References 45 publications

Compartmentation of Triacylglycerol Accumulation in Plants

Compartmentation of Triacylglycerol Accumulation in Plants

The Phosphate Fast-Responsive Genes PECP1 and PPsPase1 Affect Phosphocholine and Phosphoethanolamine Content

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

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