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Malate- and Pyruvate-Dependent Fattyacid Synthesis In Plant Physiol. (1992) 98, 1233-1238 Received for publication July 9, 1991 0032-0889/92/98/1 233/06/$01 .00/0 Accepted October 10, 1991 Malate- and Pyruvate-Dependent Fatty Acid Synthesis in Leucoplasts from Developing Castor Endosperm' Ronald G. Smith*2, David A. Gauthier, David T. Dennis3, and David H. Turpin Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4 ABSTRACT or leucoplast glycolytic enzymes are more than adequate to endosperm Leucoplasts were isolated from the endosperm of developing account for the triacylglycerol synthesis of castor castor (Ricinis communis) endosperm using a discontinuous Per- (17). However, glycolytic intermediates have not been well coil gradient. The rate of fatty acid synthesis was highest when characterized as carbon sources for fatty acid synthesis (18). malate was the precursor, at 155 nanomoles acetyl-CoA equiva- In this study, we present data regarding the kinetics and lents per milligram protein per hour. Pyruvate and acetate also exogenous cofactor requirements for fatty acid synthesis in were precursors of fatty acid synthesis, but the rates were ap- isolated leucoplast preparations using pyruvate, malate, and proximately 4.5 and 120 times less, respectively, than when acetate as carbon sources. We show that malate and pyruvate malate was the precursor. When acetate was supplied to leuco- support much higher rates of fatty acid synthesis than does plasts, exogenous ATP, NADH, and NADPH were required to acetate and the metabolism of both these substrates alleviates obtain maximal rates of fatty acid synthesis. In contrast, the any requirement for externally added reductant. Based on the incorporation of malate and pyruvate into fatty acids did not measurement of leucoplast-associated NADP+-malic enzyme require a supply of exogenous reductant. Further, the incorpora- we suggest that malate may be a source of tion of radiolabel into fatty acids by leucoplasts supplied with activity, cytosolic radiolabeled malate, pyruvate, or acetate was reduced upon carbon for fatty acid synthesis in vivo. coincubation with cold pyruvate or malate. The data suggest that malate and pyruvate may be good in vivo sources of carbon for MATERIALS AND METHODS fatty acid synthesis and that, in these preparations, leucoplast fatty acid synthesis may be limited by activity at or downstream Plant Material of the acetyl-CoA carboxylase reaction. Castor plants (Ricinus communis L. cv Baker 296) were greenhouse grown under natural light supplemented with 16 h fluorescent light. Leucoplast Isolation Storage lipids make up 45 to 50% of the dry weight of castor bean (Ricinus communis) endosperm (9, 15). During Leucoplasts were isolated by a method similar to that development, the conversion of sucrose to triacylglycerols is reported by Boyle et al. (5). Endosperm of castor seeds, stages the major metabolic activity of this tissue (9). Dennis (11) 5 to 6 (14), were dissected, placed in homogenization buffer presented a model indicating the possible pathways of triac- (1:2, w/v), and ground with a mortar and pestle containing ylglycerol synthesis from sucrose. The model is primarily sea sand. The homogenate was filtered through four layers of based on enzyme compartmentation studies (12, 17, 22, 23, cheesecloth and centrifuged at 500g for 5 min. The superna- 27) and suggests that glycolytic intermediates may cross the tant (50.5) was centrifuged at 6000g for 10 min. The resulting leucoplast membrane and serve as carbon skeletons for fatty pellet (P6) was resuspended in 5 mL homogenization buffer acid synthesis. Acetate is another possible precursor. and layered onto a discontinuous Percoll gradient. The gra- Acetate incorporation into fatty acids has been used to dient consisted of 5 mL of 35% PBF-Percoll, 10 mL of 22% study the cofactor requirements for fatty acid biosynthesis (6, PBF-Percoll, and 7.5 mL of 10% PBF-Percoll. Each layer 16, 18, 25, 26). It is unlikely that acetate is the in vivo carbon contained 50 mM Hepes-KOH (pH 7.5), 0.4 M sorbitol, 0.4 precursor of fatty acid synthesis because of its relatively low mM EDTA, 1 mM MgCl2 (5). The gradient was centrifuged in cellular concentration and the low efficiency of acetate utili- a swing-out rotor at 9200g for 8 min. The band ofleucoplasts zation for de novo fatty acid synthesis in oil seeds (21). On at the 22 to 35% Percoll interface was collected and used the other hand, glycolytic intermediates are present in rela- directly in the subsequent experiments. The direct use of this tively large concentrations and the activities of the cytosolic fraction reduced the damage to the leucoplasts as judged by the enolase intactness assay. Supported by the Natural Sciences and Engineering Council of Canada. Determination of Leucoplast Intactness 2 Present address: Department of Biology, University College of the Cariboo, Box 3010, Kamloops, B.C., V2C 5N3, Canada. A comparison between the enolase activity in leucoplasts 'Present address: Department of Biology, Queen's University, resuspended in osmoticum in the presence or absence of Kingston, Ontario, K7L 3N6, Canada. Triton X-100 was used to determine the intactness of each 1233 1234 SMITH ET AL. Plant Physiol. Vol. 98, 1992 preparation. Enolase activity was measured using an enzy- and were then stopped with 400 AL of 0.65 N KOH. The matic-coupled assay and a dual wavelength spectrophotome- radiolabel incorporated into fatty acids was partitioned into ter (Sigma ZFP22). The assay mixture contained 50 mM Tes CHCl3 by adding 750 ,uL of CHCl3/MeOH (2:1). In the case (pH 7.5), 0.4 M sorbitol, 10 mM MgCl2, 0.05 mM NADH, 3 of '4C-substrate, the CHCl3 layer was washed three to five mM ADP, 1 mM 2-phosphoglyceric acid, 2 units pyruvate times with 750 ,L of 0.5 M KCl, mixed with Aquasol II (New kinase', and 2 units lactate dehydrogenase (final volume 600 England Nuclear), counted using a liquid scintillation counter ,uL) and the absorbance at 340 nm was followed. The propor- (LKB) and quench-corrected using an external standard. Sam- tion of "leaky" leucoplasts was taken as the ratio ofthe initial ples containing 3H were treated as above except that they were enolase activity to that following the disruption of the leuco- dried and resuspended in 250 ML of CHCl3 before adding the plasts by adding 10 ,L of 10% Triton X-100. scintillation cocktail. The CHCl3 did not quench the counting of 3H or 14C samples (data not shown). Marker Enzymes and Protein Assay [14C]CO2 release when leucoplasts were supplied with uni- formly labeled ['4C]malate was measured by incubating leu- Marker enzyme activities and protein concentrations were coplasts with 2.5 mm malate (specific activity, 1 mmol/mCi) determined for the S0.5, P6, and leucoplast fractions of each for 1 h in the center well of a sealed flask. Incubations were preparation. Acetyl-CoA carboxylase (EC 6.4.1.2), NAD-iso- stopped with 200 ML of 1.0 N HCl and left overnight. The citrate dehydrogenase (EC 1.1.1.41), and catalase (EC ['4C]CO2 released by the leucoplasts was trapped in 1 mL of 1.11.1.6) were used as marker enzymes for the leucoplast, 3-phenylethylamine placed outside the center well of the mitochondrial, and peroxisomal fractions, respectively. The incubation flask. The base was removed and mixed with 5 assay conditions for these assays are as reported elsewhere (4, mL of Aquasol II and counted as above. The incubation 8). Briefly, acetyl-CoA carboxylase was assayed by a [14C] mixture was alkalized with 200 ML of 2.5 N KOH and used HC03- technique. Samples were incubated in buffer contain- to determine the incorporation of malate into fatty acids as ing 50 mm Tris (pH 8.0), 0.5 mM MgC92, 0.5 mM MnCl2, 0.5 described above. mM DTT, 1 mm ATP, 1 mm acetyl-CoA, and 10 mM NaHCO3 (specific activity, 0.5 mmol/mCi). The incubations lasted for Malic Enzyme Assay up to 2.5 min and were stopped with ethanol/formic acid/ water (80:5:20, v/v). The samples were dried down three times The NAD- and NADP-dependent malic enzyme (EC and the dpm ofeach sample determined by liquid scintillation 1.1.1.39 and EC 1.1.1.40, respectively) activity ofthe S0.5, P6, counting. NAD-isocitrate dehydrogenase was assayed spectro- and leucoplast fractions were measured using a stopped assay. photometrically using a dual wavelength spectrophotometer Samples (100 ML) were incubated in 50 mM Hepes-NaOH (Sigma, ZFP22). The assay buffer contained 50 mM Tes (pH buffer (pH 7.0) containing 20 mm KCI, 6 mm MnCl2, 5 mM 7.5), 4 mM D,L-isocitrate, 2 mM MnSO4, and 1 mM NAD. L-malate, 0.75 mM EDTA, and 1 mm NADP+ or NAD+. Catalase activity was assayed through the production of 02 in Incubations lasted 30 min, a period of linear malic enzyme a Clark-type 02 electrode (Hansatech Ltd., King's Lynn, activity (data not shown), and the incubation stopped with England). The reaction buffer contained 100 mm potassium the addition of 100 ML of 1 N HCI. The samples were neu- phosphate (pH 7.5) and 0.3% (final concentration) H202. tralized with 5 N KOH/1 M triethanolamine. The pyruvate Protein concentrations were measured according to Brad- produced during the incubations was assayed using a standard ford (7) using a Bio-Rad assay kit and ay-globulin as a standard. enzymatic coupled technique and a dual wavelength spectro- To remove the BSA present in the homogenization buffer photometer (Sigma ZFP22) (4). The activity of NADP-malic and Percoll, the fractions were washed three times in buffer enzyme was also measured directly with a dual wavelength containing 50 mM Hepes-KOH (pH 7.5), 1 M sorbitol, and 1 spectrophotometer.
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