Phosphatidylglycerol biosynthesis in chloroplasts of Arabidopsis mutants deficient in acyl-ACP glycerol-3-phosphate acyltransferase

Plant Journal

Volumn 47, Issue 2, 2006, Pages 296-309

  Xu, Changcheng ^a   Yu, Bin ^a,b   Cornish, Adam J ^a   Froehlich, John E ^a   Benning, Christoph ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acyl ACP; ATS1; ATS2; Lysophosphatidic acid; Phosphatidic acid; Prokaryotic pathway

Indexed keywords

BIOSYNTHESIS; CATALYSIS; CHLOROPHYLL; ENZYMES; GENES; LIPIDS; RNA;

ACYLTRANSFERASE; ATS1; ATS2; COORDINATED REGULATION; PHOSPHATIDYLGLYCEROL BIOSYNTHESIS; PLASTID LIPID;

GLYCEROL;

ARABIDOPSIS PROTEIN; COMPLEMENTARY DNA; GLYCEROL 3 PHOSPHATE ACYLTRANSFERASE; PHOSPHATIDYLGLYCEROL; PLASTIDIC GLYCEROL 3 PHOSPHATE ACYLTRANSFERASE, ARABIDOPSIS; PLASTIDIC GLYCEROL-3-PHOSPHATE ACYLTRANSFERASE, ARABIDOPSIS;

ALLELE; ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CHLOROPLAST; ENDOPLASMIC RETICULUM; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; HISTOLOGY; METABOLISM; MUTATION; PHENOTYPE; RNA INTERFERENCE;

ALLELES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; DNA, COMPLEMENTARY; ENDOPLASMIC RETICULUM; ESCHERICHIA COLI; GLYCEROL-3-PHOSPHATE O-ACYLTRANSFERASE; MUTAGENESIS, INSERTIONAL; MUTATION; PHENOTYPE; PHOSPHATIDYLGLYCEROLS; RNA INTERFERENCE;

BIOSYNTHESIS; CATALYSTS; CHLOROPHYLLS; ENZYMES; GENES; GLYCEROL; LIPIDS; NUCLEIC ACIDS;

ARABIDOPSIS; VIRIDIPLANTAE;

EID: 33745655860     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2006.02790.x     Document Type: Article

References (46)

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. Arabidopsis Genome Initiative (2001) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796-815.
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. Bell, R.M. (1974) Mutants of Escherichia coli defective in membrane phospholipid synthesis: macromolecular synthesis in an sn-glycerol 3-phosphate acyltransferase Km mutant. J. Bacteriol. 117, 1065-1076.
5. Bonaventure, G., Bao, X., Ohlrogge, J. and Pollard, M. (2004) Metabolic responses to the reduction in palmitate caused by disruption of the FATB gene in Arabidopsis. Plant Physiol. 135, 1269-1279.
6. Browse, J., Warwick, N., Somerville, C.R. and Slack, C.R. (1986) Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the '16:3' plant Arabidopsis thaliana. Biochem. J. 235, 25-31.
7. Bruce, B.D., Perry, S., Froehlich, J. and Keegstra, K. (1994) In vitro import of protein into chloroplasts. In Plant Molecular Biology Manual (Gelvin, S.B. and Schilperoort, R.A., eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 1-15.
8. Cline, K., Werner-Washburne, M., Andrews, J. and Keegstra, K. (1984) Thermolysin is a suitable protease for probing the surface of intact pea chloroplasts. Plant Physiol. 75, 675-678.
9. 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.
10. Cronan, J.E., Jr and Bell, R.M. (1974) Mutants of Escherichia coli defective in membrane phospholipid synthesis: mapping of sn-glycerol 3-phosphate acyltransferase Km mutants. J. Bacteriol. 120, 227-233.
11. Dörmann, P., Hoffmann-Benning, S., Balbo, I. and Benning, C. (1995) Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyl diacylglycerol. Plant Cell, 7, 1801-1810.
12. Dörmann, P., Balbo, I. and Benning, C. (1999) Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1. Science, 284, 2181-2184.
13. Estelle, M.A. and Somerville, C. (1987) Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol. Gen. Genet. 206, 200-206.
14. Falcone, D.L., Ogas, J.P. and Somerville, C.R. (2004) Regulation of membrane fatty acid composition by temperature in mutants of Arabidopsis with alterations in membrane lipid composition. BMC Plant Biol. 4, 17.
15. 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.
16. Heath, R.J. and Rock, C.O. (1998) A conserved histidine is essential for glycerolipid acyltransferase catalysis. J. Bacteriol. 180, 1425-1430.
17. Heath, R.J. and Rock, C.O. (1999) A missense mutation accounts for the defect in the glycerol-3-phosphate acyltransferase expressed in the plsB26 mutant. J. Bacteriol. 181, 1944-1946.
18. Heinz, E. and Roughan, G. (1983) Similarities and differences in lipid metabolism of chloroplasts isolated from 18:3 and 16:3 plants. Plant Physiol. 72, 273-279.
19. Ishizaki, O., Nishida, I., Agata, K., Eguchi, G. and Murata, N. (1988) Cloning and nucleotidesequence of cDNA for the plastid glycerol-3-phosphate acyltransferase from squash. FEBS Lett. 238, 424-430.
20. Jackson, D.T., Froehlich, J.E. and Keegstra, K. (1998) The hydrophilic domain of Tic110, an inner envelope membrane component of the chloroplastic protein translocation apparatus, faces the stromal compartment. J. Biol. Chem. 273, 16583-16588.
21. Kachroo, A., Venugopal, S.C., Lapchyk, L., Falcone, D., Hildebrand, D. and Kachroo, P. (2004) Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proc. Natl Acad. Sci. USA, 101, 5152-5157.
22. Kim, H.U. and Huang, A.H. (2004) Plastid lysophosphatidyl acyltransferase is essential for embryo development in Arabidopsis. Plant Physiol. 134, 1206-1216.
23. Klaus, D., Härtel, H., Fitzpatrick, L., Froehlich, J., Hubert, J., Benning, C. and Dörmann, P. (2002) Digalactosyldiacylglycerol synthesis in chloroplasts of the Arabidopsis thaliana dgd1 mutant. Plant Physiol. 128, 885-895.
24. Kunst, L., Browse, J. and Somerville, C. (1988) Altered regulation of lipid biosynthesis in a mutant of Arabidopsis deficient in chloroplast glycerol-3-phosphate acyltransferase activity. Proc. Natl Acad. Sci. USA, 85, 4143-4147.
25. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
26. Lal, S., Choi, J.H., Shaw, J.R. and Hannah, L.C. (1999) A splice site mutant of maize activates cryptic splice sites, elicits intron inclusion and exon exclusion, and permits branch point elucidation. Plant Physiol. 121, 411-418.
27. Lazarova, G.I., Kerckhoffs, L.H., Brandstadter, J., Matsui, M., Kendrick, R.E., Cordonnier-Pratt, M.M. and Pratt, L.H. (1998) Molecular analysis of PHYA in wild-type and phytochrome A-deficient mutants of tomato. Plant J. 14, 653-662.
28. Lübeck, J., Heins, L. and Soll, J. (1997) A nuclear-coded chloroplastic inner envelope membrane protein uses a soluble sorting intermediate upon import into the organelle. J. Cell Biol. 137, 1279-1286.
29. Mongrand, S., Besoule, J.-J., Cabantous, F. and Cassagne, C. (1998) The C16:3/C18:3 fatty acid balance in photosynthetic tissues from 468 plant species. Phytochemistry, 49, 1049-1064.
30. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant 15, 473-497.
31. Murata, N. and Tasaka, Y. (1997) Glycerol-3-phosphate acyltransferase in plants. Biochim. Biophys. Acta, 1348, 10-16.
32. Murata, N., Ishizaki-Nishizawa, O., Higashi, S., Hayashi, H., Tasaka, Y. and Nishida, I. (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature, 356, 710-713.
33. Nishida, I., Tasaka, Y., Shiraishi, H. and Murata, N. (1993) The gene and the RNA for the precursor to the plastid-located glycerol-3-phosphate acyltransferase of Arabidopsis thaliana. Plant Mol. Biol. 21, 267-277.
34. Rogers, S.O. and Bendich, A.J. (1994) Extraction of total cellular DNA from plants, algae and fungi. In Plant Molecular Biology Manual (Gelvin, S.B. and Schilperoort, R.A., eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 1-8.
35. Rossak, M., Schäfer, A., Xu, N., Gage, D.A. and Benning, C. (1997) Accumulation of sulfoquinovosyl-1-O-dihydroxyacetone in a sulfolipid-deficient mutant of Rhodobacter sphaeroides inactivated in sqdC. Arch. Biochem. Biophys. 340, 219-230.
36. Roughan, P.G. and Slack, C.R. (1982) Cellular organization of glycerolipid metabolism. Annu. Rev. Plant Physiol. 33, 97-132.
37. 14C]acetate by cell-free preparations from spinach (Spinacia oleracea) leaves. Biochem. J. 188, 17-24.
38. Saba, J.D. (2004) Lysophospholipids in development: miles apart and edging in. J. Cell Biochem. 92, 967-992.
39. Sigal, Y.J., McDermott, M.I. and Morris, A.J. (2005) Integral membrane lipid phosphatases/phosphotransferases: common structure and diverse functions. Biochem. J. 387, 281-293.
40. Simpson, C.G., McQuade, C., Lyon, J. and Brown, J.W. (1998) Characterization of exon skipping mutants of the COP1 gene from Arabidopsis. Plant J. 15, 125-131.
41. Tranel, P.J., Froehlich, J., Goyal, A. and Keegstra, K. (1995) A component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway. EMBO J. 14, 2436-2446.
42. Wolter, F.P., Schmidt, R. and Heinz, E. (1992) Chilling sensitivity of Arabidopsis thaliana with genetically engineered membrane lipids. EMBO J. 11, 4685-4692.
43. Xu, C., Härtel, H., Wada, H., Hagio, M., Yu, B., Eakin, C. and Benning, C. (2002) The pgp1 locus of Arabidopsis encodes a phosphatidylglycerol synthase with impaired activity. Plant Physiol. 129, 594-604.
44. Xu, C., Fan, J., Riekhof, W., Froehlich, J.E. and Benning, C. (2003) A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis. EMBO J. 22, 2370-2379.
45. Xu, C., Fan, J., Froehlich, J., Awai, K. and Benning, C. (2005) Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis. Plant Cell, 17, 3094-3110.
46. Yu, B., Wakao, S., Fan, J. and Benning, C. (2004) Loss of plastidic lysophosphatidic acid acyltransferase causes embryo-lethality in Arabidopsis. Plant Cell Physiol. 45, 503-510.