- Research article
- Open Access
Characterization of two Arabidopsis thaliana acyltransferases with preference for lysophosphatidylethanolamine
© Stålberg et al; licensee BioMed Central Ltd. 2009
- Received: 24 October 2008
- Accepted: 16 May 2009
- Published: 16 May 2009
Two previously uncharacterized Arabidopsis genes that encode proteins with acyltransferase PlsC regions were selected for study based on their sequence similarity to a recently identified lung lysophosphatidylcholine acyltransferase (LPCAT). To identify their substrate specificity and biochemical properties, the two Arabidopsis acyltransferases, designated AtLPEAT1, (At1g80950), and AtLPEAT2 (At2g45670) were expressed in yeast knockout lines ale1 and slc1 that are deficient in microsomal lysophosphatidyl acyltransferase activities.
Expression of AtLPEAT1 in the yeast knockout ale1 background exhibited strong acylation activity of lysophosphatidylethanolamine (LPE) and lysophosphatidate (LPA) with lower activity on lysophosphatidylcholine (LPC) and lysophosphatidylserine (LPS). AtLPEAT2 had specificities in the order of LPE > LPC > LPS and had no or very low activity with LPA. Both acyltransferases preferred 18:1-LPE over 16:0-LPE as acceptor and preferred palmitoyl-CoA as acyl donor in combination with 18:1-LPE. Both acyltransferases showed no or minor responses to Ca2+, despite the presence of a calcium binding EF-hand region in AtLPEAT2. AtLPEAT1 was more active at basic pH while AtLPEAT2 was equally active between pH 6.0 – 9.0.
This study represents the first description of plant acyltransferases with a preference for LPE. In conclusion it is suggested that the two AtLPEATs, with their different biochemical and expression properties, have different roles in membrane metabolism/homoeostasis.
- Acyl Donor
- Microsomal Preparation
- Acyltransferase Activity
- Acyl Acceptor
- Calcium Binding Domain
Acyltransferases comprise several families of enzymes with diverse origins and functions. The first acyltransferase recognized to be involved in phosphatydylethanolamine synthesis was identified based on the PlsC mutant in Escherichia coli, (named after its defect in phospholipid synthesis). Over 5000 acyltransferses are annotated in the UniProtKB database with a PlsC signature . In the Arabidopsis genome, 24 proteins are encoded that contain this signature but the substrate specificity has been determined for less than 10 members. Most of the PlsC domain acyltransferases have two conserved domains NH(X)4D, (IPB002123A)  and FPEGT, (IPB002123B)  of which the former is also part of the active site. This broad family of enzymes accept at least two different acyl donors, acyl-CoA and acyl-ACP and several acyl acceptors such as glycerol-3-phosphate (G3P), and lysophospholipids and include members of 1-acyl-sn-glycerol-3-phosphate acyltransferase, tafazzin and glycerol-3-phosphate O-acyltransferase enzymes (IPR002123). Lysophosphatidic acid acyltransferases (LPAATs) of the PlsC type have been cloned and characterised from many organisms. Much more scarcely represented are lysophosphatidylethanolamine specific acyltransferses (LPEATs). However, a bifunctional acyl-ACP synthase having an acyltransferase domain of the PlsC type was shown to be involved in uptake and acylation of 1-acyl-glycerophosphoethanolamine, (1-acyl-GPE), in E. coli, . Moreover, in Synechocystis a broad acyl-ACP specificity acyltransferase with 1-acyl-glycerophosphoethanolamine activity, and with a strong preference for 16:0-ACP/lysophosphatidylglycerol, (LPG) has been well characterized, . Very recently a human LPEAT2 was cloned and shown to be expressed in brain .
In yeast, Saccharomyces cerevisiae, a novel type of acyltransferases YOR175c (ALE1) belonging to the family of membrane bound O-acyltransferases (MBOAT) has recently been shown to represent a major acyl-CoA dependent lysophospholipid acyltransferase [6–12]. Knockout of ALE1 (Δyor175c:KanMX4) results in the loss of in vitro acylation of LPC, LPE, LPI, LPG, LPS and LPA, but sufficient activity of LPAAT is still provided for de novo synthesis of phospholipids by SLC1, (PlsC type). While knockout of either ALE1 or SLC1 results in no obvious growth defect, double knockout of ale1/slc1 results in a severe growth defect  or lethality [6, 8, 12], which suggests that together the two enzymes are indispensable for the synthesis of PA. A novel plant LPAAT was identified by functional complementation of the Escherichia coli mutant PlsC by Bourgis et al.,  and in Arabidopsis a plastidic LPAAT was shown to be essential for embryo development [15, 16]. By analysis of the Arabidopsis genome and alignments of putative acyltransferases in a phylogenetic tree, fifteen Arabidopsis genes encoding proteins that had both NH(X)4D and EGT motifs were identified . Among them, At1g80950 was found, but to our knowledge was not further characterized. A second gene at locus At2g45670, less similar, was not identified, although it belongs to the same family of genes. In this study we have expressed cDNAs from these two genes in yeast ale1 and slc1 knockouts and initially characterized their biochemical functions in vitro.
Expression of the two putative lysophospholipid acyltransferases AtLPEAT1, (At1g80950) and AtLPEAT2, (At2g45670) in yeast ale1 showed that both proteins possess acyltransferase activity with long-chain acyl-CoA and lysophospholipid substrates. Time and protein dependence of reactions were determined for AtLPEAT2 with 18:1-CoA and 18:1-LPE. The correlation coefficients were 0.94, (nmol/mg/0–2 min) and 0.98, (nmol/0.5 – 2 mg/min) between the variables, indicating good linearity of the assay [see Additional file 1 and 2].
Assays with 16:0-LPE and 18:1-LPE with different combinations of 16:0-CoA and 18:1-CoA showed that both Arabidopsis acyltransferases were more active with these acyl acceptors than with LPC (Figure 2). AtLPEAT1 was more active with both LPE substrates than AtLPEAT2. Both enzymes had highest activity with 16:0-CoA and 18:1-LPE. Di-18:1-PE and di-16:0-PE were equally well synthesized as by AtLPEAT2 (Figure 2).
The possibility that the C-terminal EF-hand calcium binding domain provided regulation by calcium was tested by adding CaCl2 to the assay mixtures. However, neither of the two AtLPEATs activities was dramatically affected by this addition nor by EDTA [see Additional file 4]. Assaying pH dependency of the two Arabidopsis constructs expressed in yeast ale1 was done in 25 mM Tris buffer. In this analysis, AtLPEAT1 exhibited an almost linear increase in response at pH 6.0 – 9.0, while AtLPEAT2 had constant activities over this same pH interval (Figure 3).
Our initial attempt to characterise AtLPEAT1 and AtLPEAT2 by expression in wild-type yeast was obscured due to high background lysophosphatidylcholine acyltransferase activities of ALE1 LPCAT. However, recent cloning and characterisation of ALE1 in yeast made it possible to characterize our candidate proteins in a low background strain containing a kanMX4 knockout of this gene. Since ale1 has almost no lysophospholipid acyltransferase activities except for LPAAT, [6–8, 10–12], expression in this mutant should reflect the substrate specificities of the candidate acyltransferases. However as one of the Arabidopsis enzymes turned out to have strong dual activity with high LPAAT activity, we also decided to express the Arabidopsis acyltransferases in the yeast, SLC1 knockout. The SLC1 gene was cloned as a suppressor gene which enabled yeast to grow without sphingolipid synthesis and was shown to code for an LPAAT protein . Utilizing these yeast mutants for gal induced expression of AtLPEAT1 and AtLPEAT2 we found a remarkable difference in preference for LPA between the two enzymes. AtLPEAT1 preferred 16:0-CoA eight fold over 18:1-CoA using 16:0-LPA as an acyl acceptor. The increase of LPAAT activity was more pronounced in slc1 (8 fold), than in ale1 (2.6 fold). This selectivity of 16:0-CoA is somewhat similar to the Arabidopsis LPAAT1 (LPAT1) preference, although the acyl acceptor in their assay was 18:1-LPA, . Four other Arabidopsis LPAATs (LPAT2, LPAT3, LPAT4 and LPAT5) were later isolated and characterized for their acyl donor specificities . All four LPAATs possessed higher in vitro activity with 18:1-CoA than 16:0-CoA when expressed in wild-type yeast. AtLPEAT1 exhibited strong selectivity depending on the combination of acyl acceptor and acyl donor in the acylation of LPE and LPA. The best acceptor was 18:1-LPE in combination with 16:0-CoA. AtLPEAT2 lacked acylation capability of LPA except for a low rate of formation of di-16:0-PA. Like AtLPEAT1, AtLPEAT2 showed the highest specific activity with 18:1-LPE in combination with 16:0-CoA.
The sequence homology of AtLPEATs to mammalian LPCATs is intriguing (Figure 1B and 1C). An alignment over the region containing the PlsC domain of these evolutionarily distantly related proteins distinguishes these acyltransferases from other PlsC domain containing proteins distal of the FPEGT site. Using the FPEGT motif and an adjacent 30 aa of AtLPEAT1 in a BLAST search of the non-redundant protein database retrieved exclusively this family. As can be seen in Figure 1C AtLPEAT2 has a Glutamate (E) instead of the otherwise completely conserved Aspartate (D) in the catalytic site. The mouse lung LPCAT1, highly homologous to human, (Aytl2) and mouse/rat LPCAT, has been shown to have preference for saturated fatty acids of both acceptors and donors [22, 23], while Aytl3 a human LPEAT2 showed no such preference for acyl-CoAs . LPE was also a substrate for this enzyme, but in contrast to the two AtLPEATs it preferred LPC over LPE. The pH optimum for the mouse lung LPCAT was between 7.4 and 10, and the reaction did not require Ca2+. Neither of the two AtLPEATs required Ca2+. In contrast, the human HsLPCAT (Aytl2) exhibiting EF1 and EF2-hand domains as AtLPEAT2, was shown to be inhibited by Ca2+,  while HsLPEAT2 was not effected by Ca2+ . AtLPEAT1 had a completely different response to pH 6.0 – 9.0 while AtLPEAT2 resembled the human LPCATs by being non sensitive within that pH range.
In eukaryotes, synthesis of PE occurs by three different pathways. Decarboxylation of PS, phosphoethanolamine transfer from CDP-ethanolamine to diacylglycerol and base exchange of the headgroup, (serine with ethanolamine). In Arabidopsis, CTP:phosphorylethanolamine cytidylyltransferase, (PECT) mutants exhibit a decrease of phosphatidylethanolamine and increase in phosphatidylcholine and embryo abortion, . Both AtLPEATs were predicted to be in the secretory pathway and PE is known to be a rather specific target for plant secretory phospholipases A2 (PL A2) . This type of phospholipase requires Ca2+ for activity and has no acyl chain preference . Auxin has been shown to induce and increase the levels of free fatty acids, LPC and LPE in microsomes  and LPE is also known to retard senescence, which might be related to LPE's inhibitory effect of phospholipase D . Overexpression of AtsPL A2 in Arabidopsis results in prolonged leaf petiols and inflorescence stems and general cell elongation . Whether the AtLPEATs described in this study have a function in relation to PL A2on induced responses or in organogenesis remains to be seen. Related to developmental cues is the generation of fatty acids for membrane synthesis. In vitro acylation of PC and PE in Arabidopsis showed that the ratio of labelling of PE to PC was highly different in root and leaf and specific PE remodelling by acylation has been demonstrated to be the cause of the remodelling , AtLPEAT1 and AtLPAT2 are obvious candidates involved in such remodelling.
The specific activity (10–30 nmol product/min/mg protein) of the LPEATs in the yeast microsomes were similar or higher than other lysophosphatidyl enzymes assayed under similar conditions. The acyl acceptors used in our assays were sn-1-acyl lysophospholipids and thus acylation occurred at the sn-2 position. It should be noted that palmitoyl-CoA was found to be the best acyl donor by the two AtLPEATs despite the fact that palmitate is primarily confined to the sn-1 position of plant PE. There are substantial problems to assay the sn-1 acylation activity of lysophospholipid acyltransferases because the sn-2 lysophospholipid substrates are unstable due to rapid acyl migration to the sn-1 position. Since the positional specificity of the LPEATs were not studied in this work, we can not infer any positional preference of the enzymes and cannot rule out that an additional in-vivo acyl acceptor for the AtLPEATs in plants might be sn-2-acyl lysophospholipids.
In conclusion, backward transacylation reaction,  and/or hydrolysis of phospholipids in combination with forward lysophosphatidyl acyltransferases reaction could at least partly be maintained by the AtLPEATs described herein. The difference in expression pattern of the two AtLPEATs, together with their different biochemical properties, suggest that the two AtLPEAT homologues have partly different functions in membrane metabolism/homoeostasis. Future studies of Arabidopsis that are mutated or have overexpressed LPEAT genes are likely to give valuable information about their physiological functions.
Constructs and Strains
Two full-length cDNA clones (pda09299, pda10945) corresponding to the Arabidopsis genes At1g80950 and At2g45670 were obtained from RIKEN, . Expression of the protein coding sequence of these clones in yeast using the pYES2 gal inducible system was enabled by PCR amplification, using Pfu polymerase under standard conditions. The following oligonuceotide primers were used for amplification: At1g80950 (1) 5'gtgggtaccataatggaatcagagctcaa-3', At1g80950 (2) 5' ccaggcatgctcattcttctttctgatggaa-3', At2g45670 (1) 5' cagggtaccagaatggcggatcctgatct-3', At2g45670 (2) 5' tctcgcatgcttatgttggggccaagtcag-3'. The oligonucleotides contained 5' Kpn1 and 3' Sph1 3' restriction sites for cloning into the corresponding sites of pYES2. The generated clones in pYES2 were sequenced to confirm identity with the cDNAs and were named AtLPEAT1 (At1g80950) and AtLPEAT2 (At2g45670). Two different haploid knockout mutants of ALE1, ale1:(BY4741; Mat a; his3Δ1; leu2Δ0; lys2Δ0; ura3Δ0; YOR175c::kanMX4) and SLC1, slc1:(BY4742; Mat α; his3Δ1; leu2Δ0; lys2Δ0; ura3Δ0; YDL052c::kanMX4) a corresponding wt: (BY4742; Mat α; his3Δ1; leu2Δ0; lys2Δ0; ura3Δ0). The yeast BY-series were from euroscarf  and were transformed to achieve expression of the two Arabidopsis acyltransferase proteins. An empty vector pYES2 was used as a control.
Transgenic yeast strains containing vector constructs encoding the acyltransferases and empty vector control were pre-cultured over night in 3 ml of synthetic media containing 2% Gal without uracil. Thirty ml of synthetic media containing 2% Gal -U was inoculated from the pre-culture (all diluted to the same OD) and grown at 28°C overnight to an OD of approximately 4.0. Twenty ml of fresh media were added to cultures and incubated for an additional 4 h. The cells were spun down in 50 ml falcon tubes and the supernatant discarded. The pellets were resuspended in 3 ml extraction buffer, (20 mM Tris-HCl pH 7.6, 1 mM EDTA) and transferred to 2 ml microfuge snap cap tubes containing approximately 0.5 ml of 0.5 mm zirconia silicabeads and the cells were disrupted in a Retch bead beater 30/s, 1 × 3 minutes in pre-chilled supplies. The homogenates were centrifuged at 1000 × g for 10 min and supernatants transferred to new tubes. The tubes were washed by adding 0.85 ml extraction buffer, vortexed, centrifuged and pooled with supernatants. The supernatants were diluted with extraction buffer to 8 ml and spun at 100 000 × g, 1 hour 4°C. The pellet was carefully resuspended in 0.5 ml extraction buffer, and aliquots of 50 μl extracts, "microsomal extracts", were frozen and stored at -70°C.
Lipid analysis and assay conditions
Protein concentrations were determined by Bradford assay using fatty acid free BSA as a standard. The assay for acyltransferase reaction (final volume of 33 μl) contained, if not otherwise stated in the Figure legends; 25 mM tris-HCl pH 7.6, 0.4 M KCl, 0.75 nmol [1-14C]acyl-CoA (25000 dpm), obtained from American Radiolabeled Chemicals, St Louis, 0.25 nmol of synthetic lysophospholipids (Avanti polar lipids, inc) and microsomal preparations as amounts indicated in the Figures. 0.4 M KCl was added to avoid precipitation of acyl-CoA as cations precipitate most of palmitoyl-CoA at mM concentration. Lysophospholipids dissolved in water/ethanol 1:1, were heated briefly before adding to the assay mix. The reactions were started by adding "microsomal extract" preparations under vortexing to pre-warmed microfuge tubes containing the assay mix. The reaction was incubated at 30°C for 2 minutes and stopped by adding 133 μl 50:50:1, methanol/chloroform/acetic acid and vortexing. After addition of 13.3 μl H2O the mixture was, vortexed, centrifuged 13000 × g and the lower phase was transferred to new tube. The water phase was extracted once again by adding 66 μl chloroform. The pooled organic phases were evaporated under a stream of N2, dissolved in 15 μl chloroform and spotted on silica gel 60, 20 × 20 cm TLC plates (Merck). The TLC plates were developed to 3/4 in 85:15:10:3.5 methanol/chloroform/acetic acid/water. The phospholipids were identified by comparison to known standards and quantification was done by autoradiography on a Packard InstantImager, with Version 2.05 software, using triplicates of 1/10th of the assay mix, (without microsomal preparations), spotted after development at top of each plate. Background subtraction was done for each lane at positions where no visible spots could be seen. Synthetic lysophospholipid acyl acceptors were; 1-palmitoyl-2-hydroxy-sn-glycero-3-phosphocholine, 1-oleoyl-2-hydroxy-sn-glycero-3-phosphocholine, 1-palmitoyl-2-hydroxy-sn-glycero-3-phosphoethanolamine, 1-oleoyl-2-hydroxy-sn-glycero-3-phosphoethanolamine, 1-palmitoyl-2-hydroxy-sn-glycero-3-phosphatidate, 1-palmitoyl-2-hydroxy-sn-glycero-3-phosphoserine. Acyl donors were; palmitoyl-Coenzyme A, (16:0-CoA), oleoyl-Coenzyme A, (18:1-CoA) and corresponding radiolabeled acyl-CoAs; [14C]16:0-CoA 60 mCi/mmol 0.02 mCi/ml [14C ]18:1-CoA 55 mCi/mmol 0.1 mCi/ml.
We would like to acknowledge valuable discussions with Dr. Michael Pollard. This work was supported by United States Department of Energy Grant DE-FG02-87ER13729, VR Swedish Research Council and FORMAS Swedish Research Council.
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