Lipid trafficking between the endoplasmic reticulum and the plastid in Arabidopsis requires the extraplastidic TGD4 protein

Plant Cell

Volumn 20, Issue 8, 2008, Pages 2190-2204

  Xu, Changcheng ^a   Fan, Jilian ^a   Cornish, Adam J ^a   Benning, Christoph ^a  

^a Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 57749094124     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.108.061176     Document Type: Article

References (67)

1. Achleitner, G., Gaigg, B., Krasser, A., Kainersdorfer, E., Kohlwein, S. D., Perktold, A., Zellnig, G., and Daum, G. (1999). Association between the endoplasmic reticulum and mitochondria of yeast facilitates interorganelle transport of phospholipids through membrane contact. Eur. J. Biochem. 264: 545-553.
2. Andersson, M.X., Goksor, M., and Sandelius, A.S. (2007). Optical manipulation reveals strong attracting forces at membrane contact sites between endoplasmic reticulum and chloroplasts. J. Biol. Chem. 282: 1170-1174.
3. 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.
4. Andersson, M.X., Larsson, K.E., Tjellstrom, H., Liljenberg, C., and Sandelius, A.S. (2005). Phosphate-limited oat. The plasma membrane and the tonoplast as major targets for phospholipid-to-glycolipid replacement and stimulation of phospholipases in the plasma membrane. J. Biol. Chem. 280: 27578-27586.
5. 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.
6. Awai, K., Xu, C., Tamot, B., and Benning, C. (2006). A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking. Proc. Natl. Acad. Sci. USA 103: 10817-10822.
7. Bannai, H., Tamada, Y., Maruyama, O., Nakai, K., and Miyano, S. (2002). Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18: 298-305.
8. Batoko, H., Zheng, H.Q., Hawes, C., and Moore, I. (2000). A rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell 12: 2201-2218.
9. Bell, C.J., and Ecker, J.R. (1994). Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics 19: 137-144.
10. Benning, C. (2008). A role for lipid trafficking in chloroplast biogenesis. Prog. Lipid Res. 47: 381-389.
11. Benning, C., and Ohta, H. (2005). Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J. Biol. Chem. 280: 2397-2400.
12. Benning, C., Xu, C., and Awai, K. (2006). Non-vesicular and vesicular lipid trafficking involving plastids. Curr. Opin. Plant Biol. 9: 241-247.
13. Browse, J., and Somerville, C. (1991). Glycerolipid biosynthesis: Biochemistry and regulation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 467-506.
14. Browse, J., and Somerville, C.R. (1994). Glycerolipids. In Arabidopsis, E.M. Meyerowitz and C.R. Somerville, eds (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 881-912.
15. 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.
16. 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.
17. 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.
18. Cruz-Ramirez, A., Oropeza-Aburto, A., Razo-Hernandez, F., Ramirez-Chavez, E., and Herrera-Estrella, L. (2006). Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc. Natl. Acad. Sci. USA 103: 6765-6770.
19. Da Silva, P., Landon, C., Industri, B., Marais, A., Marion, D., Ponchet, M., and Vovelle, F. (2005). Solution structure of a tobacco lipid transfer protein exhibiting new biophysical and biological features. Proteins 59: 356-367.
20. Dörmann, P., Balbo, I., and Benning, C. (1999). Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1. Science 284: 2181-2184.
21. Dörmann, P., and Benning, C. (2002). Galactolipids rule in seed plants. Trends Plant Sci. 7: 112-118.
22. 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.
23. Ferro, M., Salvi, D., Brugiere, S., Miras, S., Kowalski, S., Louwagie, M., Garin, J., Joyard, J., and Rolland, N. (2003). Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol Cell Proteomics. 2: 325-345.
24. 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.
25. 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.
26. Gounaris, K., and Barber, J. (1983). Monogalactosyldiacylglycerol: The most abundant polar lipid in nature. Trends Biochem. Sci. 8: 378-381.
27. Hajdukiewicz, P., Svab, Z., and Maliga, P. (1994). The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25: 989-994.
28. 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.
29. 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.
30. Jaquinod, M., Villiers, F., Kieffer-Jaquinod, S., Hugouvieux, V., Bruley, C., Garin, J., and Bourguignon, J. (2007). A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol. Cell. Proteomics 6: 394-412.
31. 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.
32. Jouhet, J., Marechal, E., and Block, M.A. (2007). Glycerolipid transfer for the building of membranes in plant cells. Prog. Lipid Res. 46: 37-55.
33. Joyard, J., Block, M.A., Malherbe, A., Marechal, E., and Douce, R. (1993). Origin and synthesis of galactolipid and sulfolipid head groups. In Lipid Metabolism in Plants, T.S. Moore, ed (Boca Raton, FL: CRC Press), pp. 232-258.
34. Kader, J.-C. (1996). Lipid transfer proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 627-654.
35. 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.
36. Kjellberg, J.M., Trimborn, M., Andersson, M., and Sandelius, A.S. (2000). Acyl-CoA dependent acylation of phospholipids in the chloroplast envelope. Biochim. Biophys. Acta 1485: 100-110.
37. Kobayashi, K., Kondo, M., Fukuda, H., Nishimura, M., and Ohta, H. (2007). Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis. Proc. Natl. Acad. Sci. USA 104: 17216-17221.
38. Konieczny, A., and Ausubel, F.M. (1993). A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 4: 403-410.
39. 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.
40. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
41. Li, M., Qin, C., Welti, R., and Wang, X. (2006a). Double knockouts of phospholipases Dzeta1 and Dzeta2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol. 140: 761-770.
42. Li, M., Welti, R., and Wang, X. (2006b). Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases D zeta1 and D zeta2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiol. 142: 750-761.
43. Lichtenthaler, H.K. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic membranes. Methods Enzymol. 148: 350-382.
44. Lu, B., Xu, C., Awai, K., Jones, A.D., and Benning, C. (2007). A small ATPase protein of Arabidopsis, TGD3, involved in chloroplast lipid import. J. Biol. Chem. 282: 35945-35953.
45. Maldonado, A.M., Doerner, P., Dixon, R.A., Lamb, C.J., and Cameron, R.K. (2002). A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419: 399-403.
46. Meyer, K., Benning, G., and Grill, E. (1996). Cloning of plant genes based on the genetic map position. In Genome Mapping in Plants, A. H. Patterns, ed (New York: Academic Press), pp. 137-154.
47. Mongrand, S., Bessoule, 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.
48. Mongrand, S., Bessoule, J.J., and Cassagne, C. (1997). A reexamination in vivo of the phosphatidylcholine-galactolipid metabolic relationship during plant lipid biosynthesis. Biochem. J. 327: 853-858.
49. Mongrand, S., Cassagne, C., and Bessoule, J.J. (2000). Import of lyso-phosphatidylcholine into chloroplasts likely at the origin of eukaryotic plastidial lipids. Plant Physiol. 122: 845-852.
50. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15: 473-497.
51. Nakamura, Y., Awai, K., Masuda, T., Yoshioka, Y., Takamiya, K., and Ohta, H. (2005). A novel phosphatidylcholine-hydrolyzing phospholipase C induced by phosphate starvation in Arabidopsis. J. Biol. Chem. 280: 7469-7476.
52. Nakamura, Y., Tsuchiya, M., and Ohta, H. (2007). Plastidic phosphatidic acid phosphatases identified in a distinct subfamily of lipid phosphate phosphatases with prokaryotic origin. J. Biol. Chem. 282: 29013-29021.
53. Ohlrogge, J.B., Kuhn, D.N., and Stumpf, P.K. (1979). Subcellular localization of acyl carrier protein in leaf protoplasts of Spinacia oleracea. Proc. Natl. Acad. Sci. USA 76: 1194-1198.
54. Osteryoung, K.W., and Nunnari, J. (2003). The division of endosymbiotic organelles. Science 302: 1698-1704.
55. 14C]acetate by cell-free preparations from spinach (Spinacia oleracea) leaves. Biochem. J. 188: 17-24.
56. Roughan, P.G., and Slack, C.R. (1982). Cellular organization of glycerolipid metabolism. Annu. Rev. Plant Physiol. 33: 97-132.
57. Roughan, P.G., Thompson, G.A., and Cho, S.H. (1987). Metabolism of exogenous long-chain fatty acids by spinach leaves. Arch. Biochem. Biophys. 259: 481-496.
58. Schwacke, R., Schneider, A., van der Graaff, E., Fischer, K., Catoni, E., Desimone, M., Frommer, W.B., Flugge, U.I., and Kunze, R. (2003). ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol. 131: 16-26.
59. Sessions, A., et al. (2002). A high-throughput Arabidopsis reverse genetics system. Plant Cell 14: 2985-2994.
60. Thoma, S., Kaneko, Y., and Somerville, C. (1993). A non-specific lipid transfer protein from Arabidopsis is a cell wall protein. Plant J. 3: 427-436.
61. Vance, J.E. (1990). Phospholipid synthesis in a membrane fraction associated with mitochondria. J. Biol. Chem. 265: 7248-7256.
62. Xu, C., 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.
63. 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.
64. 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.
65. 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.
66. Xu, C., Moellering, E.R., Fan, J., and Benning, C. (2008). Mutation of a mitochondrial outer membrane protein affects chloroplast lipid biosynthesis. Plant J. 54: 163-175.
67. Yamaryo, Y., Dubots, E., Albrieux, C., Baldan, B., and Block, M.A. (2008). Phosphate availability affects the tonoplast localization of PLDzeta2, an Arabidopsis thaliana phospholipase D. FEBS Lett. 582: 685-690.