Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis

Plant Cell

Volumn 17, Issue 11, 2005, Pages 3094-3110

  Xu, Changcheng ^a   Fan, Jilian ^a   Froehlich, John E ^b   Awai, Koichiro ^a   Benning, Christoph ^a  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACIDS; LIPIDS; METABOLISM;

EMBRYO ABORTION; GALACTOLIPIDS; HOMEOSTASIS; LIPID TRANSPORTER;

PROTEINS;

FATTY ACIDS; LIPIDS; METABOLISM; PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

EID: 33646004283     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.105.035592     Document Type: Article

References (67)

1. Andersson, M.X., Kjellberg, J.M., and Sandelius, A.S. (2004). The involvement of cytosolic lipases in converting phosphatidyl choline to substrate for galactolipid synthesis in the chloroplast envelope. Biochim. Biophys. Acta 1684, 46-53.
2. Andrews, J., and Mudd, J.B. (1985), Phosphatidylglycerol synthesis in pea chloroplasts: Pathway and localization. Plant Physiol. 79, 259-265.
3. Awai, K., Marechal, E., Block, M.A., Brun, D., Masuda, T., Shimada, H., Takamiya, K., Ohta, H., and Joyard, J. (2001). Two types of MGDG synthase genes, found widely in both 16:3 and 18:3 plants, differentially mediate galactolipid syntheses in photosynthetic and nonphotosynthetic tissues in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 98, 10960-10965.
4. Benning, C., Huang, Z.H., and Gage, D.A. (1995). Accumulation of a novel glycolipid and a betaine lipid in cells of Rhodobacter sphaeroides grown under phosphate limitation. Arch. Biochem. Biophys. 317, 103-111.
5. Benning, C., and Ohta, H. (2005). Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J. Biol. Chem. 280, 2397-2400.
6. Bessoule, J.J., Testet, E., and Cassagne, C. (1995). Synthesis of phosphatidylcholine in the chloroplast envelope after import of lysophosphatidylcholine from endoplasmic reticulum membranes. Eur. J. Biochem. 228, 490-497.
7. Block, M.A., Dorne, A.J., Joyard, J., and Douce, R. (1983). Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. II. Biochemical characterization. J. Biol. Chem. 258, 13281-13286.
8. 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.
9. Browse, J., and Somerville, C. (1991). Glycerolipid biosynthesis: Biochemistry and regulation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 467-506.
10. 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.
11. Bruce, B.D., Perry, S., Froehlich, J., and Keegstra, K. (1994). In vitro import of protein into chloroplasts. In Plant Molecular Biology Manual, S.B. Gelvin and R.A. Schilperoort, eds (Boston: Kluwer Academic Publishers), pp. 1-15.
12. Cernac, A., and Benning, C. (2004). WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J. 40, 575-585.
13. 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.
14. Dörmann, P., Balbo, I., and Benning, C. (1999). Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1. Science 284, 2181-2184.
15. Dörmann, P., and Benning, C. (2002). Galactolipids rule in seed plants. Trends Plant Sci. 7, 112-118.
16. 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.
17. Douce, R., and Joyard, J. (1996). Biosynthesis of thylakoid membrane lipids. In Oxygenic Photosynthesis: The Light Reactions, D.R. Ort and C.F. Yocum, eds (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 69-101.
18. Estelle, M.A., and Somerville, C. (1987). Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol. Gen. Genet. 206, 200-206.
19. Fischer, K., Weber, A., Arbinger, B., Brink, S., Eckerskorn, C., and Flügge, U.I. (1994). The 24 kDa outer envelope membrane protein from spinach chloroplasts: Molecular cloning, in vivo expression and import pathway of a protein with unusual properties. Plant Mol. Biol. 25, 167-177.
20. Flügge, U.I. (1998). Metabolite transporters in plastids. Curr. Opin. Plant Biol. 1, 201-206.
21. Froehlich, J.E., Benning, C., and Dörmann, P. (2001). The digalactosyldiacylglycerol (DGDG) synthase DGD1 is inserted into the outer envelope membrane of chloroplasts in a manner independent of the general import pathway and does not depend on direct interaction with monogalactosyldiacylglycerol synthase for DGDG biosynthesis. J. Biol. Chem. 276, 31806-31812.
22. 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.
23. Härtel, H., Dörmann, P., and Benning, C. (2000). DGD1-independent biosynthesis of extraplastidic galactolipids following phosphate deprivation in Arabidopsis. Proc. Natl. Acad. Sci. USA 97, 10649-10654.
24. Heinz, E. (1977). Enzymatic reactions in galactolipid biosynthesis. In Lipids and Lipid Polymers in Higher Plants, M. Tevini and H.K. Lichtenthaler, eds (Berlin: Springer-Verlag), pp. 102-120.
25. 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.
26. 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,
27. Jarvis, P., Dörmann, P., Peto, C.A., Lutes, J., Benning, C., and Chory, J. (2000). Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. Proc. Natl. Acad. Sci. USA 97, 8175-8179.
28. Joyard, J., and Douce, R. (1977). Site of synthesis of phosphatidic acid and idacylglcyerol in spinach chloroplasts. Biochim. Biophys. Acta 486, 273-285.
29. Kelly, A.A., Froehlich, J.E., and Dörmann, P. (2003). Disruption of the two digalactosyldiacylglycerol synthase genes DGD1 and DGD2 in Arabidopsis reveals the existence of an additional enzyme of galactolipid synthesis. Plant Cell 15, 2694-2706.
30. Kunst, L., Browse, J., and Somerville, C. (1988). Altered regulation of lipid biosynthesis in a mutant Arabidopsis deficient in chloroplast glycerol-3-phosphate acyltransferase activity. Proc. Natl. Acad. Sci. USA 85, 4143-4147.
31. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
32. Lee, S., Park, J., and Lee, Y. (2003). Phosphatidic acid induces actin polymerization by activating protein kinases in soybean cells. Mol. Cells 15, 313-319.
33. Li, W., Li, M., Zhang, W., Welti, R., and Wang, X. (2004). The plasma membrane-bound phospholipase Ddelta enhances freezing tolerance in Arabidopsis thaliana. Nat. Biotechnol. 22, 427-433.
34. Lichtenthaler, H.K. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic membranes. Methods Enzymol. 148, 350-382.
35. Loewen, C.J., Gaspar, M.L., Jesch, S.A., Delon, C., Ktistakis, N.T., Henry, S.A., and Levine, T.P. (2004). Phospholipid metabolism regulated by a transcription factor sensing phosphatidic acid. Science 304, 1644-1647.
36. 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.
37. Malherbe, A., Block, M.A., Joyard, J., and Douce, R. (1992). Feedback inhibition of phosphatidate phosphatase from spinach chloroplast envelope membranes by diacylglycerol. J. Biol. Chem. 267, 23546-23553.
38. Mansfield, S.G., and Briarty, L.G. (1991). Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can. J. Bot. 69, 461-476.
39. Marechal, E., Block, M.A., Dorne, A.-J., and Joyard, J. (1997). Lipid synthesis and metabolism in the plastid envelope. Physiol. Plant 100, 65-77.
40. McAndrew, R.S., Froehlich, J.E., Vitha, S., Stokes, K.D., and Osteryoung, K.W. (2001). Colocalization of plastid division proteins in the chloroplast stromal compartment establishes a new functional relationship between FtsZ1 and FtsZ2 in higher plants. Plant Physiol. 127, 1656-1666.
41. Miege, C., Marechal, E., Shimojima, M., Awai, K., Block, M.A., Ohta, H., Takamiya, K., Douce, R., and Joyard, J. (1999). Biochemical and topological properties of type A MGDG synthase, a spinach chloroplast envelope enzyme catalyzing the synthesis of both prokaryotic and eukaryotic MGDG. Eur. J. Biochem. 265, 990-1001.
42. Mongrand, S., Besoule, J.-J., Cabantous, F., and Cassagne, C. (1998). The C16:3/C18:3 fatty acid balance in photosyntheitc tissues from 468 plant species. Phytochemistry 49, 1049-1064.
43. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant 15, 473-497.
44. 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.
45. Ohlrogge, J., and Browse, J. (1995). Lipid biosynthesis. Plant Cell 7, 957-970.
46. Ohnishi, J., and Yamada, M. (1982). Glycerolipid synthesis in Avena leaves during greening of etiolated seedlings III. Synthesis of a linolenoyl monogalactosyl diacylglycerol from liposomal linoleoyl-phosphatidylcholine by Avena plastids in the presence of phosphatidylcholine-exchange protein. Plant Cell Physiol. 23, 767-773.
47. Park, J., Gu, Y., Lee, Y., Yang, Z., and Lee, Y. (2004). Phosphatidic acid induces leaf cell death in Arabidopsis by activating the Rhorelated small G protein GTPase-mediated pathway of reactive oxygen species generation. Plant Physiol. 134, 129-136.
48. Pearce, M.L., and Slabas, A.R. (1998). Phosphatidate phosphatase from avocado (Persea americana): Purification, substrate specificity and possible metabolic implications for the Kennedy pathway and cell signaling in plants. Plant J. 14, 555-564.
49. Pierrugues, O., Brutesco, C., Oshiro, J., Gouy, M., Deveaux, Y., Carman, G.M., Thuriaux, P., and Kazmaier, M. (2001). Lipid phosphate phosphatases in Arabidopsis. Regulation of the AtLPP1 gene in response to stress. J. Biol. Chem. 276, 20300-20308.
50. Potocky, M., Elias, M., Profotova, B., Novotna, Z., Valentova, O., and Zarsky, V. (2003). Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 217, 122-130.
51. 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.
52. Roughan, P.G., Holland, R., and Slack, C.R. (1980). The role of chloroplasts and microsomal fractions in polar-lipid synthesis from [1-14C]acetate by cell-free preparations from spinach (Spinacia oleracea) leaves. Biochem. J. 188, 17-24.
53. Roughan, P.G., and Slack, C.R. (1982). Cellular organization of glycerolipid metabolism. Annu. Rev. Plant Physiol. 33, 97-132.
54. Sakaki, T., Saito, K., Kawaguchi, A., Kondo, N., and Yamada, M. (1990). Conversion of monogalactosyldiacylglycerols to triacylglycerols in ozone-fumigated spinach leaves. Plant Physiol. 94, 766-772.
55. Schunemann, D., Borchert, S., Flügge, U.I., and Heldt, H.W. (1993). ADP/ATP translocator from pea root plastids (comparison with translocators from spinach chloroplasts and pea leaf mitochondria). Plant Physiol. 103, 131-137.
56. Shimojima, M., Ohta, H., Iwamatsu, A., Masuda, T., Shioi, Y., and Takamiya, K. (1997), Cloning of the gene for monogalactosyldiacyl-glycerol synthase and its evolutionary origin. Proc. Natl. Acad. Sci. USA 94, 333-337.
57. Silva-Filho, M.D., Wieers, M.C., Flügge, U.I., Chaumont, F., and Boutry, M. (1997). Different in vitro and in vivo targeting properties of the transit peptide of a chloroplast envelope inner membrane protein. J. Biol. Chem. 272, 15264-15269.
58. Thiery, L., Leprince, A.S., Lefebvre, D., Ghars, M.A., Debarbieux, E., and Savoure, A. (2004). Phospholipase D is a negative regulator of proline biosynthesis in Arabidopsis thaliana. J. Biol. Chem. 279, 14812-14818.
59. 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.
60. Tranel, P.J., and Keegstra, K. (1996). A novel, bipartite transit peptide targets OEP75 to the outer membrane of the chloroplastic envelope. Plant Cell 8, 2093-2104.
61. Vitha, S., Froehlich, J.E., Koksharova, O., Pyke, K.A., van Erp, H., and Osteryoung, K.W. (2003). ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15, 1918-1933.
62. Voelker, T., and Kinney, A.J. (2001). Variations in the biosynthesis of seed-storage lipids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 335-361.
63. Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949-956.
64. Weber, A., Menzlaff, E., Arbinger, B., Gutensohn, M., Eckerskorn, C., and Flügge, U.I. (1995). The 2-oxoglutarate/malate translocator of chloroplast envelope membranes: molecular cloning of a transporter containing a 12-helix motif and expression of the functional protein in yeast cells. Biochemistry 34, 2621-2627.
65. 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.
66. 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.
67. 2-induced cell death in Arabidopsis. Plant Cell 15, 2285-2295.