Phosphate Deprivation Induces Transfer of DGDG Galactolipid from Chloroplast to Mitochondria

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2004 Dec 1

PMID 15569715

Citations 81

Authors

Juliette Jouhet

Eric Marechal

Barbara Baldan

Richard Bligny

Jacques Joyard

Maryse A Block

Affiliations

Soon will be listed here.

Abstract

In many soils plants have to grow in a shortage of phosphate, leading to development of phosphate-saving mechanisms. At the cellular level, these mechanisms include conversion of phospholipids into glycolipids, mainly digalactosyldiacylglycerol (DGDG). The lipid changes are not restricted to plastid membranes where DGDG is synthesized and resides under normal conditions. In plant cells deprived of phosphate, mitochondria contain a high concentration of DGDG, whereas mitochondria have no glycolipids in control cells. Mitochondria do not synthesize this pool of DGDG, which structure is shown to be characteristic of a DGD type enzyme present in plastid envelope. The transfer of DGDG between plastid and mitochondria is investigated and detected between mitochondria-closely associated envelope vesicles and mitochondria. This transfer does not apparently involve the endomembrane system and would rather be dependent upon contacts between plastids and mitochondria. Contacts sites are favored at early stages of phosphate deprivation when DGDG cell content is just starting to respond to phosphate deprivation.

Citing Articles

Phosphorus starvation induces the synthesis of novel lipid class diacylglyceryl glucuronide and diacylglyceryl-N,N,N-trimethylhomoserine in two species of cold-adapted microalgae Raphidonema (Chlorophyta).

Suzuki H, Cuine S, Legeret B, Wijffels R, Hulatt C, Li-Beisson Y Plant J. 2025; 121(2):e17227.

PMID: 39868466 PMC: 11771548. DOI: 10.1111/tpj.17227.

Measurement of Lipid Transport in Mitochondria by the MTL Complex.

Jouhet J, Gros V, Michaud M Methods Mol Biol. 2024; 2888:167-191.

PMID: 39699731 DOI: 10.1007/978-1-0716-4318-1_12.

Organelle Interactions in Plant Cells.

Hall M, Kunjumon T, Ghosh P, Currie L, Mathur J Results Probl Cell Differ. 2024; 73:43-69.

PMID: 39242374 DOI: 10.1007/978-3-031-62036-2_3.

ER-associated VAP27-1 and VAP27-3 proteins functionally link the lipid-binding ORP2A at the ER-chloroplast contact sites.

Renna L, Stefano G, Puggioni M, Kim S, Lavell A, Froehlich J Nat Commun. 2024; 15(1):6008.

PMID: 39019917 PMC: 11255254. DOI: 10.1038/s41467-024-50425-7.

Analysis of a Super-Complex at Contact Sites Between Mitochondria and Plastids.

Michaud M Methods Mol Biol. 2024; 2776:161-176.

PMID: 38502503 DOI: 10.1007/978-1-0716-3726-5_9.

References

Raghothama K . Phosphate transport and signaling. Curr Opin Plant Biol. 2000; 3(3):182-7. View

Kelly A, Dormann P . DGD2, an arabidopsis gene encoding a UDP-galactose-dependent digalactosyldiacylglycerol synthase is expressed during growth under phosphate-limiting conditions. J Biol Chem. 2001; 277(2):1166-73. DOI: 10.1074/jbc.M110066200. View

Voelker D . New perspectives on the regulation of intermembrane glycerophospholipid traffic. J Lipid Res. 2003; 44(3):441-9. DOI: 10.1194/jlr.R200020-JLR200. View

Roughan P . Turnover of the glycerolipids of pumpkin leaves. The importence of phosphatidylcholine. Biochem J. 1970; 117(1):1-8. PMC: 1178824. DOI: 10.1042/bj1170001. View

Neuburger M, Journet E, Bligny R, Carde J, Douce R . Purification of plant mitochondria by isopycnic centrifugation in density gradients of Percoll. Arch Biochem Biophys. 1982; 217(1):312-23. DOI: 10.1016/0003-9861(82)90507-0. View

Reinsberg D, Booth P, Jegerschold C, Khoo B, Paulsen H . Folding, assembly, and stability of the major light-harvesting complex of higher plants, LHCII, in the presence of native lipids. Biochemistry. 2000; 39(46):14305-13. DOI: 10.1021/bi001365z. View

Williams J, Imperial V, Khan M, Hodson J . The role of phosphatidylcholine in fatty acid exchange and desaturation in Brassica napus L. leaves. Biochem J. 2000; 349(Pt 1):127-33. PMC: 1221129. DOI: 10.1042/0264-6021:3490127. View

Teyssier E, BLOCK M, Douce R, Joyard J . Is E37, a major polypeptide of the inner membrane from plastid envelope, an S-adenosyl methionine-dependent methyltransferase?. Plant J. 1996; 10(5):903-12. DOI: 10.1046/j.1365-313x.1996.10050903.x. View

Rebeille F, Bligny R, Douce R . Is the cytosolic pi concentration a limiting factor for plant cell respiration?. Plant Physiol. 1984; 74(2):355-9. PMC: 1066682. DOI: 10.1104/pp.74.2.355. View

10.

Mouillon J, Ravanel S, Douce R, Rebeille F . Folate synthesis in higher-plant mitochondria: coupling between the dihydropterin pyrophosphokinase and the dihydropteroate synthase activities. Biochem J. 2002; 363(Pt 2):313-9. PMC: 1222480. DOI: 10.1042/0264-6021:3630313. View

11.

Alban C, Baldet P, Douce R . 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. 1994; 300 ( Pt 2):557-65. PMC: 1138198. DOI: 10.1042/bj3000557. View

12.

Zhang M, Mileykovskaya E, Dowhan W . Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J Biol Chem. 2002; 277(46):43553-6. DOI: 10.1074/jbc.C200551200. View

13.

Bolter B, Soll J, Hill K, Hemmler R, Wagner R . A rectifying ATP-regulated solute channel in the chloroplastic outer envelope from pea. EMBO J. 1999; 18(20):5505-16. PMC: 1171619. DOI: 10.1093/emboj/18.20.5505. View

14.

Kelly A, Froehlich J, Dormann P . Disruption of the two digalactosyldiacylglycerol synthase genes DGD1 and DGD2 in Arabidopsis reveals the existence of an additional enzyme of galactolipid synthesis. Plant Cell. 2003; 15(11):2694-706. PMC: 280572. DOI: 10.1105/tpc.016675. View

15.

Douce R . Site of biosynthesis of galactolipids in spinach chloroplasts. Science. 1974; 183(4127):852-3. DOI: 10.1126/science.183.4127.852. View

16.

Vance J . Phospholipid synthesis in a membrane fraction associated with mitochondria. J Biol Chem. 1990; 265(13):7248-56. View

17.

Dorne A, Joyard J, BLOCK M, Douce R . Localization of phosphatidylcholine in outer envelope membrane of spinach chloroplasts. J Cell Biol. 1985; 100(5):1690-7. PMC: 2113847. DOI: 10.1083/jcb.100.5.1690. View

18.

Lamattina L, Gonzalez D, Gualberto J, Grienenberger J . Higher plant mitochondria encode an homologue of the nuclear-encoded 30-kDa subunit of bovine mitochondrial complex I. Eur J Biochem. 1993; 217(3):831-8. DOI: 10.1111/j.1432-1033.1993.tb18311.x. View

19.

Essigmann B, Guler S, Narang R, Linke D, Benning C . 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 U S A. 1998; 95(4):1950-5. PMC: 19220. DOI: 10.1073/pnas.95.4.1950. View

20.

Voelker D . Characterization of phosphatidylserine synthesis and translocation in permeabilized animal cells. J Biol Chem. 1990; 265(24):14340-6. View