Abstract
Jatropha curcas L. is a perennial, drought-resistant, and non-food oilseed crop. The fatty acid composition of seed oil, especially the ratio of 16- to 18-carbon fatty acids, has a direct impact on the biodiesel quality. In plants, fatty acid chain lengths are mainly determined by the plastidial fatty acid synthase complex which includes three β-ketoacyl-acyl carrier protein synthases (KASs), KASI, KASII, and KASIII. The KASIII is thought to play a rate-limiting role in fatty acid synthesis. Here, we report the functional characterization of a putative JcKASIII gene from Jatropha curcas using Arabidopsis thaliana L. as model system. The transcripts of JcKASIII were detected in all tissues examined and increased in seeds. Overexpression of JcKASIII in Arabidopsis led to an increased content of palmitic acid and a higher ratio of 16- to 18-carbon fatty acids. Moreover, functional analysis of JcAKSIII in kasI or kasII knock down Arabidopsis mutants revealed that the composition of seed oil changed. Taken together, these results suggest that heterologous JcKASIII could function as one of the major regulators of fatty acid composition.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- ACP:
-
acyl carrier protein
- CN:
-
cetane number
- DAF:
-
days after flowering
- DAS:
-
days after sowing
- FA:
-
fatty acid
- FAD:
-
fatty acid desaturase
- FAS:
-
fatty acid synthesis
- KAS:
-
β-ketoacyl-acyl carrier protein synthase
- RT-PCR:
-
reverse transcription PCR
- SAD:
-
stearoyl-ACP desaturase
- VIGS:
-
virus-induced gene silencing
- WT:
-
wild type
References
Abbadi, A., Brummel, M., Spener, F.: Knockout of the regulatory site of 3-ketoacyl-ACP synthase III enhances short- and medium-chain acyl-ACP synthesis. — Plant J. 24: 1–9, 2000.
Bamgboye, A., Hansen, A.: Prediction of cetane number of biodiesel fuel from the fatty acid methyl ester (FAME) composition. — Int. Agrophysics 22: 21–29, 2008.
Barrero, J.M., González-Bayón, R., Del Pozo, J.C., Ponce, M.R., Micol, J.L.: INCURVATA2 encodes the catalytic subunit of DNA polymerase alpha and interacts with genes involved in chromatin-mediated cellular memory in Arabidopsis thaliana. — Plant Cell 19: 2822–38, 2007.
Becker, K., Makkar, H.P.S.: Jatropha curcas: a potential source for tomorrow’s oil and biodiesel. — Lipid Technol. 20: 104–108, 2008.
Berchmans, H.J., Hirata, S.: Biodiesel production from crude Jatropha curcas L. seed oil with a high content of free fatty acids. — Bioresource Technol. 99: 1716–1721, 2008.
Biswas, B., Kazakoff, S.H., Jiang, Q.Y., Samuel, S., Gresshoff, P.M., Scoff, P.T.: Genetic and genomic analysis of the tree legume Pongamia pinnata as a feedstock for biofuels. — Plant Genome 6: doi:10.3835/plantgenome2013.05.0015, 2013.
Chen, J., Post-Beittenmiller, D.: Molecular cloning of a cDNA encoding 3-ketoacyl-acyl carrier protein synthase III from leek. — Gene 182: 45–52, 1996.
Clough, R.G., Matthis, A.L., Barnum, S.R., Jaworski, J.G.: Purification and characterization of 3-ketoacyl-acyl carrier protein synthase-III from spinach: a condensing enzyme utilizing acetyl-coenzyme-A to initiate fatty acid synthesis. — J. biol. Chem. 267: 20992–20998, 1992.
Clough, S.J., Bent, A.F.: Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. — Plant J. 16: 735–743, 1998.
Datta, M.M., Mukherjee, P., Ghosh, B., Jha, T.B.: In vitro clonal propagation of biodiesel plant (Jatropha curcas L.). — Curr. Sci. 93: 1438–1442, 2007.
Dehesh, K., Tai, H., Edwards, P., Byrne, J., Jaworski, J.G.: Overexpression of 3-ketoacyl-acyl-carrier protein synthase III in plants reduces the rate of lipid synthesis. — Plant Physiol. 125: 1103–1114, 2001.
Durrett, T.P., Benning, C., Ohlrogge, J.: Plant triacylglycerols as feedstocks for the production of biofuels. — Plant J. 54: 593–607, 2008.
Fan, R.C., Peng, C.C., Xu, Y.H., Wang, X.F., Li, Y.: Apple sucrose transporter SUT1 and sorbitol transporter SOT6 interact with cytochrome b5 to regulate their affinity for substrate sugars. — Plant Physiol. 150: 1880–1901, 2009.
González-Mellado, D., Wettstein-Knowles, P., Garcés, R., Martínez-Force, E.; The role of β-ketoacyl-acyl carrier protein synthase III in the condensation steps of fatty acid biosynthesis in sunflower. — Planta 231: 1277–1289, 2010.
Gubitz, G.M., Mittelbach, M., Trabi, M.: Exploitation of the tropical oil seed plant Jatropha curcas L. — Bioresource Technol. 67: 73–82, 1999.
Jaworski, J.G., Clough, R.C., Barnum, S.R.: A ceruleninin sensitive short chain 3-ketoacyl-acyl carrier protein synthase in Spinacia oleracea leaves. — Plant Physiol. 90: 41–44, 1989.
Jones, A.L., Gane, A.M., Herbert, D., Willey, D., Rutter, A.J., Kille, P., Dancer, J.E., Harwood, J.L.: β-Ketoacyl-acyl carrier protein synthase III from pea (Pisum sativum L.): properties, inhibition by a novel thiolactomycin analogue and isolation of a cDNA clone encoding the enzyme. — Planta 216: 752–761, 2003.
Kim, M.J., Yang, S.W., Mao, H.Z., Veena, S.P., Yin, J.L., Chua, N.H.: Gene silencing of Sugar-dependent 1 (JcSDP1), encoding a patatin-domain triacylglycerol lipase, enhances seed oil accumulation in Jatropha curcas. — Biotechnol. Biofuels 7: 36, 2014.
Kumar, N., Anand, K.G.V., Pamidimarri, S., Sarkar, T., Reddy, M.P., Radhakrishnan, T., Kaul, T., Reddy, M.K., Sopori, S.K.: Stable genetic transformation of Jatropha curcas via Agrobacterium tumefaciens-mediated gene transfer using leaf explants. — Ind. Crop Prod. 32: 41–47, 2010.
Lai, C.Y., Cronan, J.E.: β-ketoacyl-acyl carrier protein synthase III (FabH) is essential for bacterial fatty acid synthesis. — J. biol. Chem. 278: 51494–51503, 2003.
Li, J., Li, M.R., Wu, P.Z., Tian, C.E., Jiang, H.W., Wu, G.J.: Molecular cloning and expression analysis of a gene encoding a putative β-ketoacyl-acyl carrier protein (ACP) synthase III (KAS III) from Jatropha curcas. — Tree Physiol. 28: 921–927, 2008a.
Li, M., Li, H., Jiang, H., Pan, X., Wu, G.: Establishment of an Agrobacterium-mediated cotyledon disc transformation method for Jatropha curcas. — Plant Cell Tissue Organ Cult. 92: 173–781, 2008b.
Li-Beisson, Y.H., Shorrosh, B., Beisson, F., Andersson, M.X., Arondel, V., Bates, P.D., Baud, S., Bird, D., Debono, A., Durrett, T.P.: Acyl-lipid Metabolism. — In: Somerville, C.R., Meyerowitz, E.M (ed.): The Arabidopsis Book. Pp. 1–4. American Society of Plant Biologists, Rockville 2010.
Lu, W., Wei, Q., Tang, L., Yan, F., Chen, F.: Induction of callus from Jatropha curcas and rapid propagation. — Chin. J. appl. environ. Biol. 9: 127–130, 2003.
Luo, T., Peng, S.M., Deng, W.Y., Man, D.W., Xu, Y., Xiao, M., Chen, F.: Characterization of a new stearoyl-acyl carrier protein desaturase gene from Jatropha curcas. — Biotechnol. Lett. 28: 657–662, 2006.
Maghuly, F., Laimer, M.: Jatropha curcas, a biofuel crop: functional genomics for understanding metabolic pathways and genetic improvement. — Biotechnol. J. 8: 1172–1182, 2013.
Nishida, I.: Plastid metabolic pathways for fatty acid metabolism. — In: Daniell, H., Chase, C. (ed.): Mol. Biol. Biotechnol. Plant Organelles. Pp. 543–564. Springer, Dordrecht 2004.
Pan, J.L., Fu, Q.T., Xu, Z.F.: Agrobacterium tumefaciensmediated transformation of biofuel plant Jatropha curcas using kanamycin selection. — Afr. J. Biotechnol. 9: 6477–6481, 2010.
Qiu, Z.B., Wang, Y.F., Zhu, A.J., Peng, F.L., Wang, L.S.: Exogenous sucrose can enhance tolerance of Arabidopsis thaliana seedlings to salt stress. — Biol. Plant. 58: 611–617, 2014.
Qu, J., Mao, H.Z., Chen, W., Gao, S.Q., Bai, Y.N., Sun, Y.W., Geng, Y.F., Ye, J.: Development of marker-free transgenic Jatropha plants with increased levels of seed oleic acid. — Biotechnol. Biofuels. 5: 10, 2012.
Shimakata, T., Stumpf, P.K.: Isolation and function of spinach leaf β-ketoacyl-[acyl-carrier-protein] synthases. — Proc. nat. Acad. Sci. USA 79: 5808–5812, 1982.
Shrivastava, S., Banerjee, M.: In vitro clonal propagation of physic nut (Jatropha curcas L): influence of additives. — Int. J. Integr. Biol. 3: 73–77, 2008.
Slabaugh, M.B., Tai, H., Jaworski, J.G., Knapp, S.J.: cDNA clones encoding β-ketoacyl-acyl carrier protein synthase III from Cuphea wrightii. — Plant Physiol. 108: 443–444, 1995.
Stoll, C., Luhs, W., Zarhloul, M.K., Brummel, M., Spener, F., Friedt, W.: Knockout of KASIII regulation changes fatty acid composition in canola (Brassica napus). — Eur. J. Lipid Sci. Technol. 108: 277–286, 2006.
Tai, H., Post-Beittenmiller, D., Jaworski, J.G.: Cloning of a cDNA encoding 3-ketoacyl-acyl carrier protein synthase III from Arabidopsis. — Plant Physiol. 106: 801–802, 1994.
Tai, H.Y., Jaworski, J.G.: 3-Ketoacyl-acyl carrier protein synthase-III from spinach (Spinacia oleracea) is not similar to other condensing enzymes of fatty acid synthase. — Plant Physiol. 103: 1361–1367, 1993.
Takami, T., Shibata, M., Kobayashi, Y., Shikanai, T.: De novo biosynthesis of fatty acids plays critical roles in the response of the photosynthetic machinery to low temperature in Arabidopsis. — Plant Cell Physiol. 51: 1265–1275, 2010.
Thepsamran, N., Thepsithar, C., Thongpukdee, A.: In vitro induction of shoots and roots from Jatropha curcas L. explants. — J. Hort. Sci. Biotech. 83: 106–112, 2008.
Verwoert. I., Linden, V.K.H., Walsh, M.C., Nijkamp, H.J., Stuitje, A.R.: Modification of Brassica napus seed oil by expression of the Escherichia coli fabH gene, encoding 3-ketoacyl-acyl carrier protein synthase III. — Plant mol. Biol. 27: 875–886, 1995.
Wei, Q., Li, J., Zhang, L., Wu, P., Chen, Y., Li, M., Jiang, H., Wu, G.: Cloning and characterization of a β-ketoacyl-acyl carrier protein synthase II from Jatropha curcas. — J. Plant Physiol. 169: 816–824, 2012.
Wu, P.Z., Li, J., Wei, Q., Zeng, L., Chen, Y.P., Li, M.R., Jiang, H.W., Wu, G.J.: Cloning and functional characterization of an acyl-acyl carrier protein thioesterase (JcFATB1) from Jatropha curcas. — Tree Physiol. 29: 1299–1305, 2009.
Ye, J., Geng, Y.F., Zhang, B.P., Mao, H.Z., Qu, J., Chua, N.H.: The Jatropha FT ortholog is a systemic signal regulating growth and flowering time. — Biotechnol. Biofuels 7: 91, 2014a.
Ye, J., Hong, Y., Qu, J., Wang, C.: Improvement of Jatropha oil by Genetic Transformation. — Springer, New York 2012.
Ye, J., Qu, J., Bui, H.T.N., Chua, N.H.: Rapid analysis of Jatropha curcas gene functions by virus-induced gene silencing. — Plant Biotechnol. J. 7: 964–976, 2009.
Ye, J., Qu, J., Mao, H.Z., Ma, Z.G., Rahman, N.E.B., Bai, C., Chen, W., Jiang, S.Y., Ramachandran, S., Chua, N.H.: Engineering geminivirus resistance in Jatropha curcus. — Biotechnol. Biofuels. 7: 149, 2014b.
Zhang, X.R., Henriques, R., Lin, S.S., Niu, Q.W., Chua, N.H.: Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. — Nat. Protools 1: 1–6, 2006.
Zong, H., Wang, S., Ouyang, C., Deng, X.L., Li, L., Li, J.Q., Chen, F.: Agrobacterium-mediated transformation of Jatropha curcas young leaf explants with lateral shootinducing factor (LIF). — Int. J. Agr. Biol. 12: 891–896, 2010.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Acknowledgments: We are grateful to Dr. Yaoguang Liu and Dr. Chuxiong Zhuang for discussions and suggestions in the manuscript. This work was supported by the National Natural Science Foundation of China (grant Nos. 30771759 and 31170636 to Changcao Peng and 30972388 to Xiaoyang Chen) and the Natural Science Foundation of Guangdong Province (grant Nos. 9351064201000002 and 7118121 to Xiaoyang Chen).
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Yu, N., Xiao, W.F., Zhu, J. et al. The Jatropha curcas KASIII gene alters fatty acid composition of seeds in Arabidopsis thaliana . Biol Plant 59, 773–782 (2015). https://doi.org/10.1007/s10535-015-0555-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10535-015-0555-5