Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria

Journal of Cell Biology

Volumn 167, Issue 5, 2004, Pages 863-874

  Jouhet, Juliette ^a   Maréchal, Eric ^a   Baldan, Barbara ^b   Bligny, Richard ^a   Joyard, Jacques ^a   Block, Maryse A ^a  

^a CNRS   (France)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DIGALACTOSYLDIGLYCERIDE; GALACTOSE; PHOSPHATE; PHOSPHOLIPID; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; CONTROLLED STUDY; ELECTRON MICROSCOPY; LIPID ANALYSIS; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; PLANT CELL; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE;

ARABIDOPSIS; CELLS, CULTURED; CHLOROPLASTS; FOOD DEPRIVATION; GALACTOLIPIDS; INTRACELLULAR MEMBRANES; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; PHOSPHATES; PHOSPHOLIPIDS; PHOSPHORUS; TRANSPORT VESICLES;

ARABIDOPSIS;

EID: 10344232677     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200407022     Document Type: Article

References (51)

1. Achleitner, G., B. Gaigg, A. Krasser, E. Kainersdorfer, S.D. Kohlwein, A. Perktold, G. Zellnig, and G. Daum. 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. Alban, C., P. Baldet, and R. Douce. 1994. Localization and characterization of two structurally different forms of acetyl-CoA carboxylase in young pea leaves, of which one is sensitive to aryloxyphenoxypropionate herbicides. Biochem. J. 300:557-565.
3. Andersson, M.X., M.H. Stridh, K.E. Larsson, C. Liljenberg, and A.S. Sandelius. 2003. Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett. 537:128-132.
4. Ardail, D., F. Lerme, and P. Louisot. 1991. Involvement of contact sites in phosphatidylserine import into liver mitochondria. J. Biol. Chem. 266: 7978-7981.
5. Awai, K., E. Maréchal, M.A. Block, D. Brun, T. Masuda, H. Shimada, K. Takamiya, H. Ohta, and J. Joyard. 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. Axelos, M., C. Curie, L. Mazzolini, C. Bardet, and B. Lescure. 1992. A protocol for transient gene expression in Arabidopsis thaliana protoplasts isolated from cell suspension cultures. Plant Physiol. Biochem. 30:123-128.
7. Bligh, E.G., and W.J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
8. Block, M.A., A.J. Dorne, J. Joyard, and R. Douce. 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.
9. Bolter, B., J. Soll, K. Hill, R. Hemmler, and R. Wagner. 1999. A rectifying ATP-regulated solute channel in the chloroplastic outer envelope from pea. EMBO J. 18:5505-5516.
10. Broglie, R.M., C.N. Hunter, P. Delepelaire, R.A. Niederman, N.H. Chua, and R.K. Clayton. 1980. Isolation and characterization of the pigment-protein complexes of Rhodopseudomonas sphaeroides by lithium dodecyl sulfate/polyacrylamide gel electrophoresis. Proc. Natl. Acad. Sci. USA. 77:87-91.
11. Carter, H.E., R.H. McCluer, and E.D. Slifer. 1956. Lipids of wheat flour. I. Characterization of galactosylglycerol components. J. Am. Chem. Soc. 78:3735-3738.
12. Dorne, A.J., M.A. Block, J. Joyard, and R. Douce. 1982. The galactolipid: galactolipid galactosyltransferase is located on the outer surface of the outer chloroplast envelope. FEES Lett. 145:30-34.
13. Dorne, A.J., J. Joyard, M.A. Block, and R. Douce. 1985. Localization of phosphatidylcholine in outer envelope membrane of spinach chloroplasts. J. Cell Biol. 100:1690-1697.
14. Douce, R. 1974. Site of galactolipid synthesis in spinach chloroplasts. Science. 183:852-853.
15. Douce, R. 1985. Mitochondria in Higher Plants: Structure, Function and Biogenesis. Academic Press Inc., NY. 322 pp.
16. Essigmann, B., S. Güler, R.A. Narang, D. Linke, and C. Benning. 1998. Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 95:1950-1955.
17. Folch, J., M. Lees, and G.A. Sloane-Stanley. 1957. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226:497-509.
18. Froehlich, J.E., C. Benning, and P. Dormann. 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.
19. Härtel, H., and C. Benning. 2000. Can digalactosyldiacylglycerol substitute for phosphatidylcholine upon phosphate deprivation in leaves and roots of Arabidopsis? Biochem. Soc. Trans. 28:729-732.
20. Härtel, H., B. Essigmann, H. Lokstein, S. Hoffmann-Benning, M. Peters-Kottig, and C. Benning. 1998. The phospholipid-deficient phoI mutant of Arabidopsis thaliana is affected in the organization, but not in the light acclimation, of the thylakoid membrane. Biochim. Biophys. Acta. 1415:205-218.
21. Härtel, H., P. Dormann, and C. Benning. 2000. DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis. Proc. Natl. Acad. Sci. USA. 97:10649-10654.
22. Harwood, J.L. 1987. Phosphoglycerides of mitochondrial membranes. In Methods in Enzymology. Vol. 148. L. Packer and R. Douce, editors. Academic Press, Inc., London. 475-485.
23. 2-fixation mechanisms. Bot. Acta. 103:32-38.
24. Jouhet, J., E. Maréchal, R. Bligny, J. Joyard, and M.A. Block. 2003. Transient increase of phosphatidylcholine in plant cells in response to phosphate deprivation. FEBS Lett. 544:63-68.
25. Joyard, J., E. Maréchal, M.A. Block, and R. Douce. 1996. Plant galactolipids and sulfolipid. Structure, distribution and biosynthesis. In Membranes: Specialized Function in Plants. M. Smallwood, P. Knox, and D.J. Bowles, editors. BIOS Scientific Publishers, Oxford, UK. 179-194.
26. Kelly, A.A., and P. Dormann. 2002. DGD2, an Arabidopsis gene encoding a UDP-galactose-dependent digalactosyldiacylglycerol synthase is expressed during growth under phosphate-limiting conditions. J. Biol. Chem. 277:1166-1173.
27. Kelly, A.A., J.E. Froehlich, and P. Dormann. 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.
28. Klaus, D., H. Hartel, L.M. Fitzpatrick, J.E. Froehlich, J. Hubert, C. Henning, and P. Dormann. 2002. Digalactosyldiacylglycerol synthesis in chloroplasts of the Arabidopsis dgdI mutant. Plant Physiol. 128:885-895.
29. Kojima, M., K. Seki, M. Ohnishi, S. Ito, and Y. Fujino. 1990. Structure of novel glyceroglycolipids in Adzuki bean (Vigna angularis) seeds. Biochem. Cell Biol. 68:59-64.
30. Lamattina, L., D. Gonzalez, J. Gualberto, and J.M. Grienenberger. 1993. Higher plant mitochondria encode an homologue of the nuclear-encoded 30-kDa subunit of bovine mitochondrial complex I. Eur. J. Biochem. 217:831-838.
31. Lowry, H., N.J. Rosebrough, A.L. Farr, and R.J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
32. Maréchal, E., N. Azzouz, C.S. de Macedo, M.A. Block, J.E. Feagin, R.T. Schwarz, and J. Joyard. 2002. Synthesis of chloroplast galactolipids in apicomplexan parasites. Eukaryot. Cell. 1:653-656.
33. Mouillon, J.M., S. Ravanel, R. Douce, and F. Rébeillé. 2002. Folate synthesis in higher-plant mitochondria: coupling between the dihydropterin pyrophosphokinase and the dihydropteroate synthase activities. Biochem. J. 363:313-319.
34. Neuburger, M., E.P. Journet, R. Bligny, J.P. Carde, and R. Douce. 1982. Purification of plant mitochondria by isopycnic centrifugation in density gradients of Percoll. Arch. Biochem. Biophys. 217:312-323.
35. Norberg, P., and C. Liljenberg. 1991. Lipids of plasma membranes prepared from oat root cells. Plant Physiol. 96:1136-1141.
36. Pfeiffer, K., V. Gohil, R.A. Stuart, C. Hunte, U. Brandt, M.L. Greenberg, and H. Schagger. 2003. Cardiolipin stabilizes respiratory chain supercomplexes. J. Biol. Chem. 278:52873-52880.
37. Raghothama, K.G. 1999. Phosphate acquisition. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:665-693.
38. Raghothama, K.G. 2000. Phosphate transport and signaling. Curr. Opin. Plant Biol. 3:182-187.
39. Rébeillé, F., R. Bligny, and R. Douce. 1984. Is the cytosolic Pi concentration a limiting factor for plant cell respiration? Plant Physiol. 74:355-359.
40. Reinsberg, D., P.J. Booth, C. Jegerschold, B.J. Khoo, and H. Paulsen. 2000. Folding, assembly, and stability of the major light-harvesting complex of higher plants, LHCII, in the presence of native lipids. Biochemistry. 39: 14305-14313.
41. Roughan, G. 1970. Turnover of the glycerolipids of pumpkin leaves. The importance of phosphatidylcholine. Biochem. J. 117:1-8.
42. Teyssier, E., M.A. Block, R. Douce, and J. Joyard. 1996. Is E37, a major polypeptide of the inner membrane from plastid envelope, an S-adenosyl methionine-dependent methyltransferase? Plant J. 10:903-912.
43. Vallon, O., F.-A. Wollman, and J. Olive. 1986. Lateral distribution of the main protein complexes of the photosynthetic apparatus in Chlamydomonas reinhardtii and in spinach: an immunocytochemical study using intact thylakoid membranes and a PSII enriched membrane. Photobiochem. Photobiophys. 12:203-220.
44. van Besouw, A., and J.F. Wintermans. 1978. Galactolipid formation in chloroplast envelopes. I. Evidence for two mechanisms in galactosylation. Biochim. Biophys. Acta. 529:44-53.
45. Vance, J.E, 1990. Phospholipid synthesis in a membrane fraction associated with mitochondria. J. Biol. Chem. 265:7248-7256.
46. Voelker, D.R. 1990. Characterization of phosphatidylserine synthesis and translocation in permeabilized animal cells. J. Biol Chem. 265:14340-14346.
47. Voelker, D.R. 2003. New perspectives on the regulation of intermembrane glycerophospholipid traffic. J. Lipid Res. 44:441-449.
48. Werhahn, W., A. Niemeyer, L. Jansch, V. Kruft, U.K. Schmitz, and H. Braun. 2001. Purification and characterization of the preprotein translocase of the outer mitochondrial membrane from Arabidopsis. Identification of multiple forms of TOM20. Plant Physiol. 125:943-954.
49. Williams, J.P., V. Imperial, M.U. Khan, and J.N. Hodson. 2000. The role of phosphatidylcholine in fatty acid exchange and desaturation in Brassica napus L. leaves. Biochem. J. 349:127-133.
50. Xu, C.C., J.L. Fan, W. Riekhof, J.E. Froehlich, and C. Benning. 2003. A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis. EMBO J. 22:2370-2379.
51. Zhang, M., E. Mileykovskaya, and W. Dowhan. 2002. Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J. Biol. Chem. 277:43553-43556.