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Effect of the Expression and Knockdown of Citrate Synthase Gene on Carbon Flux During Triacylglycerol Biosynthesis by Green Algae Chlamydomonas Reinhardtii

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Effect of the Expression and Knockdown of Citrate Synthase Gene on Carbon Flux During Triacylglycerol Biosynthesis by Green Algae Chlamydomonas Reinhardtii Deng et al. BMC Biochemistry 2013, 14:38 http://www.biomedcentral.com/1471-2091/14/38 RESEARCH ARTICLE Open Access Effect of the expression and knockdown of citrate synthase gene on carbon flux during triacylglycerol biosynthesis by green algae Chlamydomonas reinhardtii Xiaodong Deng2, Jiajia Cai1 and Xiaowen Fei1* Abstract Background: The regulation of lipid biosynthesis is essential in photosynthetic eukaryotic cells. This regulation occurs during the direct synthesis of fatty acids and triacylglycerols (TAGs), as well as during other controlling processes in the main carbon metabolic pathway. Results: In this study, the mRNA levels of Chlamydomonas citrate synthase (CrCIS) were found to decrease under nitrogen-limited conditions, which suggests suppressed gene expression. Gene silencing by RNA interference (RNAi) was conducted to determine whether CrCIS suppression affected the carbon flux in TAG biosynthesis. Results showed that the TAG level increased by 169.5%, whereas the CrCIS activities in the corresponding transgenic algae decreased by 16.7% to 37.7%. Moreover, the decrease in CrCIS expression led to the increased expression of TAG biosynthesis-related genes, such as acyl-CoA:diacylglycerol acyltransferase and phosphatidate phosphatase. Conversely, overexpression of CrCIS gene decreased the TAG level by 45% but increased CrCIS activity by 209% to 266% in transgenic algae. Conclusions: The regulation of CrCIS gene can indirectly control the lipid content of algal cells. Our findings propose that increasing oil by suppressing CrCIS expression in microalgae is feasible. Keywords: Citrate synthase, Triacylglycerol biosynthesis, RNAi interference, Overexpression, Chlamydomonas reinhardtii, Nitrogen deprivation Background formation of high lipid production and high cell-density Considering that fossil fuel resources are limited, the im- cultures. These processes are crucial in genetic strain im- portance of conserving energy and saving the environ- provement, as well as in the future cultivation of commer- ment is gaining increased interest. Microalgae biodiesel, cial and industrial microalgae. a crucial renewable biomass energy that uses solar energy The substrate competition hypothesis was proposed by to fix CO2 into biomass, is the most promising alternative Sugimoto et al. and Chen et al. [1-3]. According to this to fossil fuels. However, studies on lipid metabolism in hypothesis, the lipids and proteins of seeds compete for the eukaryotic, single-celled, photosynthetic microalgae are same substrate, i.e., pyruvate, which is a product of glycoly- limited compared with those on oil crops. Basic know- sis. Phosphoenolpyruvate carboxylase (PEPC; EC4.1.1.31) ledge on microalgae is less than that of crops, such as rice, catalyzes the formation of oxaloacetate (OAA) from phos- wheat, and corn. With the intensification of microalgae- phoenolpyruvate (PEP), and then enters the tricarboxylic derived biodiesel research at the global scale, more re- (TCA) cycle to provide the substrate and energy needed searchers are focusing on the mechanism underlying the for protein synthesis. Meanwhile, acetyl–CoA carboxylase (ACCase) catalyzes the formation of acetyl coenzyme A from pyruvate, and then enters the fatty acid synthesis * Correspondence: [email protected] 1School of Science, Hainan Medical College, Haikou 571101, China pathway. Hence, photosynthetic carbon flux tends to Full list of author information is available at the end of the article © 2013 Deng et al.; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Deng et al. BMC Biochemistry 2013, 14:38 Page 2 of 11 http://www.biomedcentral.com/1471-2091/14/38 synthesize proteins or lipids depending on the relative Results activity of PEPC and ACCase. Using antisense RNA tech- Cloning of CrCIS gene and bioinformatics analysis nology to suppress PEPC activity, they obtained stable, An approximately 1500 bp DNA fragment of CrCIS high-oil rape seed lines and high-oil soybean lines whose gene full-length CDS was amplified, cloned, and se- lipid contents increased by 6.4% to 18%. Citrate synthase quenced, exhibiting 100% homology with Chlamydomo- (CIS; E.C. 2.3.3.1) is common within various organisms. nas CIS gene (Protein ID194915). Using the BLAST CIS isozymes exhibit diverse subcellular localization pat- programs and the Chlamydomonas CIS gene as entries, terns, and are involved in crucial physiological metabolic we obtained the CrCIS orthologous genes from the pathways. CIS, which is located in the mitochondria, is a NCBI database. The amino acid sequence alignment of rate-limiting enzyme during the first step of the TCA cycle. the CIS orthologous genes was created using ClustalW Through this step, CIS forms citroyl–CoA by catalyzing (http://www.genome.jp/tools/clustalw/). The phylogenetic the reaction of acetyl–CoA. Currently, biological, func- tree of the CIS orthologous genes is presented in Figure 1. tional, and applied research regarding CIS in plants mainly All listed CIS orthologous genes contained the citrate syn- focus on the following aspects. First, crops are stimulated thase function domain. The predicted subcellular location to secrete citric acids through CIS gene overexpression, of CrCIS (by Euk-mPLoc 2.0) was within the mitochon- which can activate hard-soluble P in soil to increase soil drion (http://www.csbio.sjtu.edu.cn/bioinf/euk-multi-2/). phosphorus utilization. In this context, Tong et al. cloned a CIS gene from rape and detected the gene expression mRNA level of CrCIS under N sufficient and N limited under stressful conditions [4]. Correspondingly, Hu et al. conditions bred a low-phosphorus resistant stain by overexpressing To determine the mRNA levels of the CrCIS under N- CIS gene into rice; the rice exhibited rapid root growth sufficient and N-limited conditions, 50 mL of cultivated and high secretion of citric acid [5]. Second, CIS may in- Chlamydomonas (2 × 106 cells/mL) was collected through crease cell resistance to aluminum toxicity. Citric acid centrifugation. After washing with HSM-N medium, the forms a complex with Al3+. This complex exhibits either cells were suspended and half of them were transferred to low toxicity or non-toxicity. The overexpression of CIS a new 50 mL of HSM and HSM-N medium for further in alfalfa evidently strengthens the tolerance of the plant cultivation. Algal cells harvested at 24, 48, 72, or 96 h were to acidic soil and aluminum toxicity [6]. Third, CIS ex- used for RNA extraction. We quantitatively determined pression is related to organic acid accumulation during the expression of CrCIS gene in these samples through re- fruit ripening [7]. Under this aspect, Zhang et al. pro- verse transcription followed by real-time polymerase chain vided evidence that the citric acid content of pineapple reaction (PCR). Results presented in Figure 2 exhibit the fruit is positively correlated with CIS activity during difference in lipid accumulation of cells in the two condi- pineapple maturation [8]. Studies on CIS in microalgae tions; cells accumulated three to six times more lipids are rarely reported compared with those in vascular under the N-limited condition than under the N-sufficient plants and animals. As early as the 1970s, Barrie et al. condition. Interestingly, CrCIS mRNA was undetectable published a study on CIS in microalgae. They detected under the N-limited condition. Thus, we further deter- CIS activity in four kinds of Cyanophyta, whose activity mined whether the decline in the mRNA of CrCIS levels is inhibited by factors such as α-ketoglutaric acid, nico- influenced the increase in lipid accumulation. tinamide adenine dinucleotide phosphate, and ATP; this inhibition is speculated to lead fixed carbon flux to lipid Silencing of CrCIS gene increases triacylglycerol (TAG) synthesis [9]. content in C. reinhardtii We have confirmed that existing studies have not To determine the relationship between CrCIS expression demonstrated any evidence that CIS gene expression and lipid accumulation, we examined the effects of the and regulation are related to cellular lipid accumulation. artificial silencing of CrCIS gene on the lipid content of Accordingly, this study aimed to determine whether such C. reinhardtii. Based on the CrCIS (194915) sequences relationship exists. The mRNA abundances of CrCIS and of the gene retrieved from the JGI C. reinhardtii v4.0 data- lipid accumulation were detected under plus/minus nitro- base, we designed primers (Additional file 1: Table S1) to gen conditions in Chlamydomonas reinhardtii CC124. amplify the fragment of the coding region of CrCIS.The Knockdown by RNAi and overexpression of CrCIS gene DNA fragments were subcloned and then used to gener- were then performed in Chlamydomonas to determine ate CrCIS RNAi constructs pMaa7IR/CrCIS IR. More the effect of overexpression or inhibition of CrCIS on than 120 positive transformants were obtained after cellular carbon flux and lipid accumulation. Further- transforming the silencing construct into C. reinhardtii more, the results of this study can contribute in es- CC425. Three transgenic algae were selected to measure tablishing the relationship of lipid accumulation with the lipid content and mRNA levels of the targeted gene. carbon flux distribution. Strains transformed with the vector
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