Extraplastidial cytidinediphosphate diacylglycerol synthase activity is required for vegetative development in Arabidopsis thaliana

Plant Journal

Volumn 75, Issue 5, 2013, Pages 867-879

  Zhou, Yonghong ^a   Peisker, Helga ^b   Weth, Agnes ^a   Baumgartner, Werner ^a   Dörmann, Peter ^b   Frentzen, Margrit ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Arabidopsis; cytidinediphosphate diacylglycerol synthase; membrane lipid composition; phosphatidylglycerol; phosphatidylinositol; seedling lethal

Indexed keywords

ARABIDOPSIS; MEMBRANE LIPID COMPOSITION; PHOSPHATIDYLGLYCEROLS; PHOSPHATIDYLINOSITOL; SEEDLING LETHAL; SYNTHASES;

BIOCHEMISTRY; BIOSYNTHESIS; CELL MEMBRANES; CELL PROLIFERATION; GENES; PHOSPHOLIPIDS;

GLYCEROL;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA; PROKARYOTA;

1,2-DIACYLGLYCEROL; ARABIDOPSIS PROTEIN; CHOLINEPHOSPHOTRANSFERASE; DIACYLGLYCEROL; NUCLEOTIDYLTRANSFERASE; PHOSPHATIDATE CYTIDYLYLTRANSFERASE; PHOSPHATIDYLGLYCEROL; PHOSPHATIDYLINOSITOL;

ARABIDOPSIS; ARTICLE; CYTIDINEDIPHOSPHATE DIACYLGLYCEROL SYNTHASE; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIPID METABOLISM; MEMBRANE LIPID COMPOSITION; METABOLISM; MUTATION; PHENOTYPE; PHYSIOLOGY; PLASTID; SEEDLING; SEEDLING LETHAL; THYLAKOID;

ARABIDOPSIS; CYTIDINEDIPHOSPHATE DIACYLGLYCEROL SYNTHASE; MEMBRANE LIPID COMPOSITION; PHOSPHATIDYLGLYCEROL; PHOSPHATIDYLINOSITOL; SEEDLING LETHAL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DIACYLGLYCEROL CHOLINEPHOSPHOTRANSFERASE; DIGLYCERIDES; LIPID METABOLISM; MUTATION; NUCLEOTIDYLTRANSFERASES; PHENOTYPE; PHOSPHATIDYLINOSITOLS; PLASTIDS; SEEDLING; THYLAKOIDS;

EID: 84883246189     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12248     Document Type: Article

References (57)

1. Alonso, J.M., Stepanova, A.N., Leisse, T.J., et al. (2003) Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
2. Andrews, J., and, Mudd, J.B., (1985) Phosphatidylglycerol synthesis in pea chloroplasts pathway and localization. Plant Physiol., 79, 259-265.
3. Babiychuk, E., Müller, F., Eubel, H., Braun, H.P., Frentzen, M., and, Kushnir, S., (2003) Arabidopsis phosphatidylglycerophosphate synthase 1 is essential for chloroplast differentiation, but is dispensable for mitochondrial function. Plant J., 33, 899-909.
4. Beisson, F., Koo, A.J.K., Ruuska, S., Schwender, J., Pollard, M., Thelen, J.J., Paddock, T., Salas, J.J., Savage, L., and, Milcamps, A., (2003) Arabidopsis genes involved in acyl lipid metabolism. A 2003 census of the candidates, a study of the distribution of expressed sequence tags in organs, and a web-based database. Plant Physiol., 132, 681-697.
5. Buseman, C.M., Tamura, P., Sparks, A.A., Baughman, E.J., Maatta, S., Zhao, J., Roth, M.R., Esch, S.W., Shah, J., and, Williams, T.D., (2006) Wounding stimulates the accumulation of glycerolipids containing oxophytodienoic acid and dinor-oxophytodienoic acid in Arabidopsis leaves. Plant Physiol., 142, 28-39.
6. Castelli, V., Aury, J.M., Jaillon, O., Wincker, P., Clepet, C., Menard, M., Cruaud, C., Quétier, F., Scarpelli, C., and, Schächter, V., (2004) Whole genome sequence comparisons and "full-length" cDNA sequences: a combined approach to evaluate and improve Arabidopsis genome annotation. Genome Res., 14, 406-413.
7. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J., 16, 735-743.
8. Curtis, M.D., and, Grossniklaus, U., (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol., 133, 462-469.
9. Delhaize, E., Hebb, D.M., Richards, K.D., Lin, J.M., Ryan, P.R., and, Gardner, R.C., (1999) Cloning and expression of a wheat (Triticum aestivum L.) phosphatidylserine synthase cDNA. J. Biol. Chem., 274, 7082-7088.
10. Devaiah, S.P., Roth, M.R., Baughman, E., Li, M., Tamura, P., Jeannotte, R., Welti, R., and, Wang, X., (2006) Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a phospholipase Dα1 knockout mutant. Phytochemistry, 67, 1907-1924.
11. Dowhan, W., (1997) CDP-diacylglycerol synthase of microorganisms. Biochim. Biophys. Acta, 1348, 157-165.
12. Fischer, W., Heinz, E., and, Zeus, M., (1973) The suitability of lipase from Rhizopus arrhizus delemar for analysis of fatty acid distribution in dihexosyl diglycerides, phospholipids and plant sulfolipids. Hoppe Seylers Z. Physiol. Chem., 354, 1115-1123.
13. Frentzen, M., (2004) Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation. Curr. Opin. Plant Biol., 7, 270-276.
14. Froehlich, J.E., Wilkerson, C.G., Ray, W.K., McAndrew, R.S., Osteryoung, K.W., Gage, D.A., and, Phinney, B.S., (2003) Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. J. Proteome Res., 2, 413-425.
15. Gao, J., Ajjawi, I., Manoli, A., Sawin, A., Xu, C., Froehlich, J.E., Last, R.L., and, Benning, C., (2009) FATTY ACID DESATURASE4 of Arabidopsis encodes a protein distinct from characterized fatty acid desaturases. Plant J., 60, 832-839.
16. Gillaspy, G.E., (2011) The cellular language of myo-inositol signaling. New Phytol, 192, 823-839.
17. Griebau, R., and, Frentzen, M., (1994) Biosynthesis of phosphatidylglycerol in isolated mitochondria of etiolated mung bean (Vigna radiata L.) seedlings. Plant Physiol., 105, 1269-1274.
18. Hagio, M., Sakurai, I., Sato, S., Kato, T., Tabata, S., and, Wada, H., (2002) Phosphatidylglycerol is essential for the development of thylakoid membranes in Arabidopsis thaliana. Plant Cell Physiol., 43, 1456-1464.
19. Haselier, A., Akbari, H., Weth, A., Baumgartner, W., and, Frentzen, M., (2010) Two closely related genes of Arabidopsis encode plastidial cytidinediphosphate diacylglycerol synthases essential for photoautotrophic growth. Plant Physiol., 153, 1372-1384.
20. Heazlewood, J.L., Tonti-Filippini, J., Verboom, R.E., and, Millar, A.H., (2005) Combining experimental and predicted datasets for determination of the subcellular location of proteins in Arabidopsis. Plant Physiol., 139, 598-609.
21. Heazlewood, J.L., Verboom, R.E., Tonti-Filippini, J., Small, I., and, Millar, A.H., (2007) SUBA: the Arabidopsis subcellular database. Nucleic Acids Res., 35, D213-D218.
22. Inglis-Broadgate, S.L., Ocaka, L., Banerjee, R., Gaasenbeek, M., Chapple, J.P., Cheetham, M.E., Clark, B.J., Hunt, D.M., and, Halford, S., (2005) Isolation and characterization of murine Cds (CDP-diacylglycerol synthase) 1 and 2. Gene, 356, 19-31.
23. Karimi, M., Inzé, D., and, Depicker, A., (2002) GATEWAY™ vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci., 7, 193-195.
24. Karimi, M., Depicker, A., and, Hilson, P., (2007) Recombinational cloning with plant gateway vectors. Plant Physiol., 145, 1144-1154.
25. Kleppinger-Sparace, K.F., and, Moore, Jr.T.S., (1985) Biosynthesis of cytidine 5'-diphosphate-diacylglycerol in endoplasmic reticulum and mitochondria of castor bean endosperm. Plant Physiol., 77, 12-15.
26. Kopka, J., Ludewig, M., and, Muller-Rober, B., (1997) Complementary DNAs encoding eukaryotic-type cytidine-5 [prime]-diphosphate-diacylglycerol synthases of two plant species. Plant Physiol., 113, 997-1002.
27. Löfke, C., Ischebeck, T., Konig, S., Freitag, S., and, Heilmann, I., (2008) Alternative metabolic fates of phosphatidylinositol produced by phosphatidylinositol synthase isoforms in Arabidopsis thaliana. Biochem. J., 413, 115-124.
28. Lykidis, A., and, Jackowski, S., (2000) Regulation of mammalian cell membrane biosynthesis. Prog. Nucleic Acid Res. Mol. Biol., 65, 361-393.
29. Lykidis, A., Jackson, P.D., Rock, C.O., and, Jackowski, S., (1997) The role of CDP-diacylglycerol synthetase and phosphatidylinositol synthase activity levels in the regulation of cellular phosphatidylinositol content. J. Biol. Chem., 272, 33402-33409.
30. Maclean, J., Koekemoer, M., Olivier, A., Stewart, D., Hitzeroth, I., Rademacher, T., Fischer, R., Williamson, A.L., and, Rybicki, E., (2007) Optimization of human papillomavirus type 16 (HPV-16) L1 expression in plants: comparison of the suitability of different HPV-16 L1 gene variants and different cell-compartment localization. J. Gen. Virol., 88, 1460-1469.
31. Maliga, P., Sz-Breznovits, Á., and, Marton, L., (1973) Streptomycin-resistant plants from callus culture of haploid tobacco. Nature, 244, 29-30.
32. Moore, Jr.T.S., (1982) Phospholipid biosynthesis. Annu. Rev. Plant Physiol., 33, 235-259.
33. Müller, F., and, Frentzen, M., (2001) Phosphatidylglycerophosphate synthases from Arabidopsis thaliana. FEBS Lett., 509, 298-302.
34. Munnik, T., and, Vermeer, J.E., (2010) Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. Plant Cell Environ., 33, 655-669.
35. Nerlich, A., Von Orlow, M., Rontein, D., Hanson, A.D., and, Dörmann, P., (2007) Deficiency in phosphatidylserine decarboxylase activity in the psd1 psd2 psd3 triple mutant of Arabidopsis affects phosphatidylethanolamine accumulation in mitochondria. Plant Physiol., 144, 904-914.
36. Pan, W., Pham, V.N., Stratman, A.N., et al. (2012) CDP-diacylglycerol synthetase-controlled phosphoinositide availability limits VEGFA signaling and vascular morphogenesis. Blood, 120, 489-498.
37. Roughan, P., Slack, C., and, Holland, R., (1978) Generation of phospholipid artefacts during extraction of developing soybean seeds with methanolic solvents. Lipids, 13, 497-503.
38. Sakurai, T., Satou, M., Akiyama, K., Iida, K., Seki, M., Kuromori, T., Ito, T., Konagaya, A., Toyoda, T., and, Shinozaki, K., (2005) RARGE: a large-scale database of RIKEN Arabidopsis resources ranging from transcriptome to phenome. Nucleic Acids Res., 33, D647-D650.
39. Sato, N., Hagio, M., Wada, H., and, Tsuzuki, M., (2000) Requirement of phosphatidylglycerol for photosynthetic function in thylakoid membranes. Proc. Natl Acad. Sci. USA, 97, 10655-10660.
40. Schlame, M., Rua, D., and, Greenberg, M.L., (2000) The biosynthesis and functional role of cardiolipin. Prog. Lipid Res., 39, 257.
41. Seki, M., Narusaka, M., Kamiya, A., Ishida, J., Satou, M., Sakurai, T., Nakajima, M., Enju, A., Akiyama, K., and, Oono, Y., (2002) Functional annotation of a full-length Arabidopsis cDNA collection. Science, 296, 141-145.
42. Seki, M., Carninci, P., Nishiyama, Y., Hayashizaki, Y., and, Shinozaki, K., (2003) High-efficiency cloning of Arabidopsis full-length cDNA by biotinylated CAP trapper. Plant J., 15, 707-720.
43. Shen, H., Heacock, P.N., Clancey, C.J., and, Dowhan, W., (1996) The CDS1 gene encoding CDP-diacylglycerol synthase in Saccharomyces cerevisiae is essential for cell growth. J. Biol. Chem., 271, 789-795.
44. Sparkes, I.A., Runions, J., Kearns, A., and, Hawes, C., (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat. Protoc., 1, 2019-2025.
45. Vance, J.E., and, Steenbergen, R., (2005) Metabolism and functions of phosphatidylserine. Prog. Lipid Res., 44, 207-234.
46. Volta, M., Bulfone, A., Gattuso, C., Rossi, E., Mariani, M., Consalez, G., Zuffardi, O., Ballabio, A., Banfi, S., and, Franco, B., (1999) Identification and characterization of CDS2, a mammalian homolog of the drosophila CDP-diacylglycerol synthase gene. Genomics, 55, 68-77.
47. Welti, R., Li, W., Li, M., Sang, Y., Biesiada, H., Zhou, H.E., Rajashekar, C., Williams, T.D., and, Wang, X., (2002) Profiling membrane lipids in plant stress responses. J. Biol. Chem., 277, 31994-32002.
48. Williams, J., Khan, M., and, Wong, D., (1995) A simple technique for the analysis of positional distribution of fatty acids on di-and triacylglycerols using lipase and phospholipase A2. J. Lipid Res., 36, 1407-1412.
49. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., and, Provart, N.J., (2007) An "electronic fluorescent pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE, 2, e718.
50. Wu, L., Niemeyer, B., Colley, N., Socolich, M., and, Zuker, C.S., (1995) Regulation of PLC-mediated signalling in vivo by CDP-diacylglycerol synthase. Nature, 373, 216-222.
51. Xu, C., Hartel, H., Wada, H., Hagio, M., Yu, B., Eakin, C., and, Benning, C., (2002) The pgp1 mutant locus of Arabidopsis encodes a phosphatidylglycerolphosphate synthase with impaired activity. Plant Physiol., 129, 594-604.
52. Xu, C., Fan, J., Froehlich, J.E., Awai, K., and, Benning, C., (2005) Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis. Plant Cell, 17, 3094-3110.
53. Xu, C., Yu, B., Cornish, A.J., Froehlich, J.E., and, Benning, C., (2006) Phosphatidylglycerol biosynthesis in chloroplasts of Arabidopsis mutants deficient in acyl-ACP glycerol-3-phosphate acyltransferase. Plant J., 47, 296-309.
54. Xue, H.W., Chen, X., and, Mei, Y., (2009) Function and regulation of phospholipid signalling in plants. Biochem. J., 421, 145.
55. Yamaoka, Y., Yu, Y., Mizoi, J., Fujiki, Y., Saito, K., Nishijima, M., Lee, Y., and, Nishida, I., (2011) Phosphatidylserine synthase1 is required for microspore development in Arabidopsis thaliana. Plant J., 67, 648-661.
56. Zinser, E., and, Daum, G., (1995) Isolation and biochemical characterization of organelles from the yeast, Saccharomyces cerevisiae. Yeast, 11, 493-536.
57. Zuo, J., Niu, Q.W., and, Chua, N.H., (2000) An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J., 24, 265-273.