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PMID: 9738969 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Review

The role of lipids in plastid protein transport.

Plant molecular biology ·Vol. 38 ·No. 1-2 ·1998-09-00 ·Pages 223-46

Bruce BD

Abstract

The elaborate compartmentalization of plant cells requires multiple mechanisms of protein targeting and trafficking. In addition to the organelles found in all eukaryotes, the plant cell contains a semi-autonomous organelle, the plastid. The plastid is not only the most active site of protein transport in the cell, but with its three membranes and three aqueous compartments, it also represents the most topologically complex organelle in the cell. The chloroplast contains both a protein import system in the envelope and multiple protein export systems in the thylakoid. Although significant advances have identified several proteinaceous components of the protein import and export apparatuses, the lipids found within plastid membranes are also emerging as important players in the targeting, insertion, and assembly of proteins in plastid membranes. The apparent affinity of chloroplast transit peptides for chloroplast lipids and the tendency for unsaturated MGDG to adopt a hexagonal II phase organization are discussed as possible mechanisms for initiating the binding and/or translocation of precursors to plastid membranes. Other important roles for lipids in plastid biogenesis are addressed, including the spontaneous insertion of proteins into the outer envelope and thylakoid, the role of cubic lipid structures in targeting and assembly of proteins to the prolamellar body, and the repair process of D1 after photoinhibition. The current progress in the identification of the genes and their associated mutations in galactolipid biosynthesis is discussed. Finally, the potential role of plastid-derived tubules in facilitating macromolecular transport between plastids and other cellular organelles is discussed.

MeSH Terms
Biological Transport Intracellular Membranes/metabolism Lipid Metabolism Lipids/physiology Models, Biological Plant Proteins/metabolism Plastids/metabolism
Chemicals
Lipids Plant Proteins
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Bruce B D
Center for Legume Research and Department of Biochemistry and Cellular & Molecular Biology, University of Tennessee, Knoxville 37996, USA. [email protected]
References (137)
137 references, click to expand
  1. Protein Import into and Sorting inside the Chloroplast Are Independent Processes.
    Plant Cell. 1990 May;2(5):479-494 PMID: 12354964
  2. A new chloroplast protein import intermediate reveals distinct translocation machineries in the two envelope membranes: energetics and mechanistic implications.
    J Cell Biol. 1996 Jan;132(1-2):63-75 PMID: 8567731
  3. A model for the packing of lipids in bilayer membranes.
    Biochim Biophys Acta. 1975 Apr 21;389(1):13-19 PMID: 1138904
  4. Identification of a mitochondrial receptor complex required for recognition and membrane insertion of precursor proteins.
    Nature. 1990 Dec 13;348(6302):610-6 PMID: 2174514
  5. Mitochondrial Hsp70/MIM44 complex facilitates protein import.
    Nature. 1994 Oct 27;371(6500):768-74 PMID: 7935837
  6. Mitochondrial contact sites. Lipid composition and dynamics.
    J Biol Chem. 1990 Nov 5;265(31):18797-802 PMID: 2172233
  7. Topogenic signals in integral membrane proteins.
    Eur J Biochem. 1988 Jul 1;174(4):671-8 PMID: 3134198
  8. A novel property of a mitochondrial presequence. Its ability to induce cardiolipin-specific interbilayer contacts which are dissociated by a transmembrane potential.
    FEBS Lett. 1993 Jul 26;327(2):172-6 PMID: 8392951
  9. Membrane insertion and lateral mobility of synthetic amphiphilic signal peptides in lipid model membranes.
    Biochim Biophys Acta. 1991 Jul 22;1071(2):123-48 PMID: 1854792
  10. Chloroplasts and Mitochondria in Living Plant Cells: Cinephotomicrographic Studies.
    Science. 1962 Oct 19;138(3538):434-6 PMID: 17794918
  11. 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. 1994 May;25(2):167-77 PMID: 8018867
  12. Degradation of the 32 kD Herbicide Binding Protein in Far Red Light.
    Plant Physiol. 1987 Jun;84(2):348-52 PMID: 16665442
  13. The signal peptide.
    J Membr Biol. 1990 May;115(3):195-201 PMID: 2197415
  14. An Arabidopsis thaliana cDNA encoding PS II-X, a 4.1 kDa component of photosystem II: a bipartite presequence mediates SecA/delta pH-independent targeting into thylakoids.
    FEBS Lett. 1996 Jul 22;390(2):175-8 PMID: 8706853
  15. Lipid polymorphism and the functional roles of lipids in biological membranes.
    Biochim Biophys Acta. 1979 Dec 20;559(4):399-420 PMID: 391283
  16. Synthetic analogues of a transit peptide inhibit binding or translocation of chloroplastic precursor proteins.
    J Biol Chem. 1991 Jun 25;266(18):11882-9 PMID: 2050684
  17. The structure and thermotropic properties of pure 1,2-diacylgalactosylglycerols in aqueous systems.
    Biochim Biophys Acta. 1981 Feb 23;663(2):380-9 PMID: 7213776
  18. Regulation of lipid polymorphism is essential for the viability of phosphatidylethanolamine-deficient Escherichia coli cells.
    J Biol Chem. 1994 Nov 18;269(46):28670-5 PMID: 7961817
  19. The phase behavior of lipids in photosynthetic membranes.
    J Bioenerg Biomembr. 1987 Dec;19(6):605-24 PMID: 3320039
  20. Molecular characterization of PsbW, a nuclear-encoded component of the photosystem II reaction center complex in spinach.
    Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8930-4 PMID: 7568046
  21. Mapping of the protein import machinery in the mitochondrial outer membrane by crosslinking of translocation intermediates.
    Nature. 1992 Jan 2;355(6355):84-7 PMID: 1530986
  22. Transport of proteins across the endoplasmic reticulum membrane.
    Science. 1992 Nov 6;258(5084):931-6 PMID: 1332192
  23. Current views on chloroplast protein import and hypotheses on the origin of the transport mechanism.
    J Bioenerg Biomembr. 1990 Dec;22(6):789-810 PMID: 2092038
  24. Effects of lipid packing on polymorphic phase behavior and membrane properties.
    Proc Natl Acad Sci U S A. 1989 Aug;86(15):5825-9 PMID: 2762300
  25. Sequence analysis and protein import studies of an outer chloroplast envelope polypeptide.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5778-82 PMID: 2377616
  26. The full length of a mitochondrial presequence is required for efficient monolayer insertion and interbilayer contact formation.
    Mol Membr Biol. 1994 Jul-Sep;11(3):159-64 PMID: 7742880
  27. The transit sequence of a chloroplast precursor protein reorients the lipids in monogalactosyl diglyceride containing bilayers.
    FEBS Lett. 1994 Aug 15;350(1):104-8 PMID: 8062905
  28. Synthesis of mono- and digalactosyldiacylglycerol in isolated spinach chloroplasts.
    Plant Physiol. 1988 Mar;86(3):971-7 PMID: 16666019
  29. Lipid and peptide specificities in signal peptide--lipid interactions in model membranes.
    Biochim Biophys Acta. 1990 Aug 24;1027(2):155-62 PMID: 2168756
  30. The Critical Requirement for Linolenic Acid Is Pollen Development, Not Photosynthesis, in an Arabidopsis Mutant.
    Plant Cell. 1996 Mar;8(3):403-416 PMID: 12239389
  31. Domain structure of mitochondrial and chloroplast targeting peptides.
    Eur J Biochem. 1989 Apr 1;180(3):535-45 PMID: 2653818
  32. Galactosyltransferases involved in galactolipid biosynthesis are located in the outer membrane of pea chloroplast envelopes.
    Plant Physiol. 1983 Feb;71(2):366-72 PMID: 16662832
  33. Dynamics of the photosystem II reaction center.
    Cell. 1989 Jan 27;56(2):241-6 PMID: 2643478
  34. Biosynthesis and desaturation of prokaryotic galactolipids in leaves and isolated chloroplasts from spinach.
    Plant Physiol. 1991 May;96(1):144-52 PMID: 16668143
  35. Interaction of peptides corresponding to mitochondrial presequences with membranes.
    J Biol Chem. 1991 Nov 15;266(32):21693-9 PMID: 1834660
  36. A consensus nomenclature for the protein-import components of the chloroplast envelope.
    Trends Cell Biol. 1997 Aug;7(8):303-4 PMID: 17708964
  37. The effects of galactolipid depletion on the structure of a photosynthetic membrane.
    J Cell Biol. 1986 Oct;103(4):1337-47 PMID: 3771638
  38. Genetic Enhancement of the Ability to Tolerate Photoinhibition by Introduction of Unsaturated Bonds into Membrane Glycerolipids.
    Plant Physiol. 1997 Oct;115(2):551-559 PMID: 12223823
  39. Membrane packing geometry of diphytanoylphosphatidylcholine is highly sensitive to hydration: phospholipid polymorphism induced by molecular rearrangement in the headgroup region.
    Biophys J. 1997 Aug;73(2):870-7 PMID: 9251804
  40. The chloroplast-targeting domain of plastocyanin transit peptide can form a helical structure but does not have a high affinity for lipid bilayers.
    Eur J Biochem. 1992 Jul 15;207(2):671-5 PMID: 1633818
  41. A receptor component of the chloroplast protein translocation machinery.
    Science. 1994 Dec 23;266(5193):1989-92 PMID: 7801125
  42. Pilus assembly by Agrobacterium T-DNA transfer genes.
    Science. 1996 Aug 23;273(5278):1107-9 PMID: 8688097
  43. Mitochondrial membrane contact sites of yeast. Characterization of lipid components and possible involvement in intramitochondrial translocation of phospholipids.
    J Biol Chem. 1991 Jun 5;266(16):10047-9 PMID: 2037561
  44. Targeting of proteins to the thylakoids by bipartite presequences: CFoII is imported by a novel, third pathway.
    EMBO J. 1994 Mar 15;13(6):1310-7 PMID: 8137815
  45. Transit sequence-dependent binding of the chloroplast precursor protein ferredoxin to lipid vesicles and its implications for membrane stability.
    FEBS Lett. 1995 Mar 13;361(1):35-40 PMID: 7890037
  46. The lipidic particle as an intermediate structure in membrane fusion processes and bilayer to hexagonal HII transitions.
    Biochim Biophys Acta. 1980 Aug 14;600(3):620-4 PMID: 7407134
  47. Conformations of signal peptides induced by lipids suggest initial steps in protein export.
    Science. 1986 Jul 11;233(4760):206-8 PMID: 2941862
  48. Low-temperature phase behaviour of the major plant leaf lipid monogalactosyldiacylglycerol.
    Biochim Biophys Acta. 1992 Jun 11;1107(1):77-85 PMID: 1616928
  49. Substrate-dependent transport of the NADPH:protochlorophyllide oxidoreductase into isolated plastids.
    Plant Cell. 1995 Feb;7(2):161-72 PMID: 7756827
  50. Control of topology and mode of assembly of a polytopic membrane protein by positively charged residues.
    Nature. 1989 Oct 5;341(6241):456-8 PMID: 2677744
  51. Role of the carboxy terminus of polypeptide D1 in the assembly of a functional water-oxidizing manganese cluster in photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: assembly requires a free carboxyl group at C-terminal position 344.
    Biochemistry. 1992 Nov 10;31(44):10859-71 PMID: 1420199
  52. In vitro synthesis and processing of a putative precursor for the small subunit of ribulose-1,5-bisphosphate carboxylase of Chlamydomonas reinhardtii.
    Proc Natl Acad Sci U S A. 1977 Mar;74(3):1082-5 PMID: 265554
  53. Arabidopsis mutants deficient in polyunsaturated fatty acid synthesis. Biochemical and genetic characterization of a plant oleoyl-phosphatidylcholine desaturase.
    J Biol Chem. 1992 Jan 25;267(3):1502-9 PMID: 1730697
  54. Thylakoid membranes: the translational site of chloroplast DNA-regulated thylakoid polypeptides.
    Arch Biochem Biophys. 1984 Dec;235(2):562-70 PMID: 6517602
  55. Photoinhibition of Photosystem II. Inactivation, protein damage and turnover.
    Biochim Biophys Acta. 1993 Jul 5;1143(2):113-34 PMID: 8318516
  56. Polymorphic regulation of membrane phospholipid composition in Escherichia coli.
    J Biol Chem. 1993 Jun 15;268(17):12427-33 PMID: 8509382
  57. MOM22 is a receptor for mitochondrial targeting sequences and cooperates with MOM19.
    EMBO J. 1995 Sep 1;14(17):4204-11 PMID: 7556061
  58. A constituent of the chloroplast import complex represents a new type of GTP-binding protein.
    Plant J. 1995 Mar;7(3):401-11 PMID: 7757113
  59. Isolation of components of the chloroplast protein import machinery.
    Science. 1994 Nov 11;266(5187):1007-12 PMID: 7973649
  60. Signal sequences.
    Biochemistry. 1989 Feb 7;28(3):923-30 PMID: 2653440
  61. Functional domains of the ferredoxin transit sequence involved in chloroplast import.
    J Biol Chem. 1995 Feb 24;270(8):3882-93 PMID: 7876133
  62. Molecular aspects of plastid envelope biochemistry.
    Eur J Biochem. 1991 Aug 1;199(3):489-509 PMID: 1868841
  63. In vitro synthesis and assembly of photosystem II proteins of spinach chloroplasts.
    Arch Biochem Biophys. 1986 Feb 1;244(2):517-27 PMID: 2418785
  64. Formation of inverted micelles in dispersions of mixed galactolipids.
    Nature. 1981 Oct 8;293(5832):488-90 PMID: 7312028
  65. Evidence for SecA- and delta pH-independent insertion of D1 into thylakoids.
    FEBS Lett. 1995 Jul 17;368(2):263-6 PMID: 7628618
  66. Transfer of a chloroplast-bound precursor protein into the translocation apparatus is impaired after phospholipase C treatment.
    FEBS Lett. 1992 Jul 13;306(1):71-4 PMID: 1628746
  67. Unsaturation of fatty acids in membrane lipids enhances tolerance of the cyanobacterium Synechocystis PCC6803 to low-temperature photoinhibition.
    Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9959-63 PMID: 1409727
  68. Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis.
    EMBO J. 1996 Dec 2;15(23):6416-25 PMID: 8978669
  69. Hydration and the lamellar to hexagonal II phase transition of phosphatidylethanolamine.
    Biochemistry. 1986 Nov 18;25(23):7518-22 PMID: 3801431
  70. A chemically synthesized pre-sequence of an imported mitochondrial protein can form an amphiphilic helix and perturb natural and artificial phospholipid bilayers.
    EMBO J. 1986 Jun;5(6):1327-34 PMID: 3015598
  71. Insertion of the 34-kDa chloroplast protein import component, IAP34, into the chloroplast outer membrane is dependent on its intrinsic GTP-binding capacity.
    J Biol Chem. 1997 Mar 7;272(10):6614-20 PMID: 9045691
  72. Regulation of protein metabolism: Coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes.
    Proc Natl Acad Sci U S A. 1984 Mar;81(5):1380-4 PMID: 16593427
  73. From entangled membranes to eclectic morphologies: cubic membranes as subcellular space organizers.
    FEBS Lett. 1995 Aug 1;369(1):13-7 PMID: 7641875
  74. Hydration properties of lamellar and non-lamellar phases of phosphatidylcholine and phosphatidylethanolamine.
    Chem Phys Lipids. 1996 Jul 15;81(2):117-31 PMID: 8810046
  75. The phase behavior of monogalactosyl, digalactosyl, and sulphoquinovosyl diglycerides.
    Biochim Biophys Acta. 1973 Jul 18;311(4):531-44 PMID: 4738152
  76. A Comparison between Prolamellar Bodies and Prothylakoid Membranes of Etioplasts of Dark-Grown Wheat Concerning Lipid and Polypeptide Composition.
    Plant Physiol. 1984 Dec;76(4):1036-40 PMID: 16663945
  77. Efficient modulation of glucolipid enzyme activities in membranes of Acholeplasma laidlawii by the type of lipids in the bilayer matrix.
    Biochemistry. 1995 Oct 17;34(41):13381-9 PMID: 7577924
  78. Cloning of the gene for monogalactosyldiacylglycerol synthase and its evolutionary origin.
    Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):333-7 PMID: 8990209
  79. Extensive and widespread homologies between mitochondrial DNA and chloroplast DNA in plants.
    Proc Natl Acad Sci U S A. 1984 Apr;81(7):1946-50 PMID: 16593442
  80. Effect of divalent cations on lipid organization of cardiolipin isolated from Escherichia coli strain AH930.
    Biochim Biophys Acta. 1994 Jan 19;1189(2):225-32 PMID: 8292628
  81. Kinetic resolution of the incorporation of the D1 protein into photosystem II and localization of assembly intermediates in thylakoid membranes of spinach chloroplasts.
    J Biol Chem. 1996 Apr 19;271(16):9627-36 PMID: 8621638
  82. Kinetic properties of monogalactosyldiacylglycerol synthase from spinach chloroplast envelope membranes.
    J Biol Chem. 1994 Feb 25;269(8):5788-98 PMID: 8119920
  83. Chloroplast transit peptides. The perfect random coil?
    FEBS Lett. 1991 Jan 14;278(1):1-3 PMID: 1993469
  84. The recovery of photosynthesis from low-temperature photoinhibition is accelerated by the unsaturation of membrane lipids: a mechanism of chilling tolerance.
    Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8787-91 PMID: 8090724
  85. A component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway.
    EMBO J. 1995 Jun 1;14(11):2436-46 PMID: 7781598
  86. Identification of two GTP-binding proteins in the chloroplast protein import machinery.
    Science. 1994 Nov 11;266(5187):1035-9 PMID: 7973656
  87. Mitochondrial targeting sequences may form amphiphilic helices.
    EMBO J. 1986 Jun;5(6):1335-42 PMID: 3015599
  88. Further aspects of the Ca2+-dependent polymorphism of bovine heart cardiolipin.
    Biochim Biophys Acta. 1982 Dec 8;693(1):1-12 PMID: 7150583
  89. The MIM complex mediates preprotein translocation across the mitochondrial inner membrane and couples it to the mt-Hsp70/ATP driving system.
    Cell. 1995 Jun 30;81(7):1085-93 PMID: 7600576
  90. The 'positive-inside rule' applies to thylakoid membrane proteins.
    FEBS Lett. 1991 Apr 22;282(1):41-6 PMID: 2026263
  91. Presequence-mediated intermembrane contact formation and lipid flow. A model membrane study.
    Biochemistry. 1994 May 10;33(18):5589-94 PMID: 8180182
  92. Bacteriophages M13 and Pf3 tell us how proteins insert into the membrane.
    J Struct Biol. 1990 Jul-Sep;104(1-3):38-43 PMID: 2088449
  93. Purification of UDP-galactose: diacylglycerol galactosyltransferase from chloroplast envelopes of spinach (Spinacia oleracea L.).
    Planta. 1991 Jun;184(3):319-26 PMID: 24194148
  94. The synthesis and use of thionphospholipids in 31P-NRM studies of lipid polymorphism.
    Biochim Biophys Acta. 1982 Feb 23;685(2):144-52 PMID: 7059596
  95. Mitochondrial presequence inserts differently into membranes containing cardiolipin and phosphatidylglycerol.
    Biochemistry. 1995 Mar 21;34(11):3605-13 PMID: 7893657
  96. N-terminal hydrophobic residues of the G-protein ADP-ribosylation factor-1 insert into membrane phospholipids upon GDP to GTP exchange.
    Biochemistry. 1997 Apr 15;36(15):4675-84 PMID: 9109679
  97. Amphiphilicity is essential for mitochondrial presequence function.
    EMBO J. 1988 Mar;7(3):649-53 PMID: 3396537
  98. Galactolipid formation in chloroplast envelopes. I. Evidence for two mechanisms in galactosylation.
    Biochim Biophys Acta. 1978 Apr 28;529(1):44-53 PMID: 638180
  99. Protein targeting and integration signal for the chloroplastic outer envelope membrane.
    Plant Cell. 1996 Nov;8(11):2117-26 PMID: 8953775
  100. Interaction of melittin with negatively charged phospholipids: consequences for lipid organization.
    FEBS Lett. 1987 Oct 19;223(1):148-54 PMID: 3666135
  101. In vitro interaction between a chloroplast transit peptide and chloroplast outer envelope lipids is sequence-specific and lipid class-dependent.
    J Biol Chem. 1996 Dec 20;271(51):32907-15 PMID: 8955132
  102. Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids.
    Proc Natl Acad Sci U S A. 1985 Jun;82(11):3665-9 PMID: 3858841
  103. Major coat proteins of bacteriophage Pf3 and M13 as model systems for Sec-independent protein transport.
    FEMS Microbiol Rev. 1995 Aug;17 (1-2):185-90 PMID: 7669345
  104. Common principles of protein translocation across membranes.
    Science. 1996 Mar 15;271(5255):1519-26 PMID: 8599107
  105. Analysis of the hexagonal II phase and its relations to lipidic particles and the lamellar phase. A freeze-fracture study.
    Biochim Biophys Acta. 1981 Jul 20;645(2):262-9 PMID: 7272289
  106. Artificial mitochondrial presequences.
    Proc Natl Acad Sci U S A. 1986 Dec;83(23):9011-5 PMID: 3024162
  107. In vitro synthesis and assembly of photosystem II core proteins. The D1 protein can be incorporated into photosystem II in isolated chloroplasts and thylakoids.
    J Biol Chem. 1995 Oct 27;270(43):25685-95 PMID: 7592747
  108. The transit sequence mediates the specific interaction of the precursor of ferredoxin with chloroplast envelope membrane lipids.
    J Biol Chem. 1993 Feb 25;268(6):4037-42 PMID: 8440696
  109. Lipidic cubic phases: a novel concept for the crystallization of membrane proteins.
    Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14532-5 PMID: 8962086
  110. Molecular basis for membrane phospholipid diversity: why are there so many lipids?
    Annu Rev Biochem. 1997;66:199-232 PMID: 9242906
  111. The rapidly metabolized 32,000-dalton polypeptide of the chloroplast is the "proteinaceous shield" regulating photosystem II electron transport and mediating diuron herbicide sensitivity.
    Proc Natl Acad Sci U S A. 1981 Mar;78(3):1572-6 PMID: 6940173
  112. The secondary structure of the ferredoxin transit sequence is modulated by its interaction with negatively charged lipids.
    FEBS Lett. 1993 Nov 15;334(2):241-6 PMID: 8224253
  113. Induction of non-bilayer lipid structures by functional signal peptides.
    EMBO J. 1990 Mar;9(3):815-9 PMID: 2178926
  114. Mutants of Arabidopsis deficient in the synthesis of alpha-linolenate. Biochemical and genetic characterization of the endoplasmic reticulum linoleoyl desaturase.
    J Biol Chem. 1993 Aug 5;268(22):16345-51 PMID: 8102138
  115. X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases.
    Science. 1997 Sep 12;277(5332):1676-81 PMID: 9287223
  116. Direct measurement of headgroup hydration of polar lipids in inverted micelles.
    Chem Phys Lipids. 1988 Dec;49(3):179-84 PMID: 3240563
  117. Biological significance of lipid polymorphism: the cubic phases.
    Curr Opin Struct Biol. 1997 Oct;7(5):661-8 PMID: 9345624
  118. Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyl diacylglycerol.
    Plant Cell. 1995 Nov;7(11):1801-10 PMID: 8535135
  119. Chloroplast protein topogenesis: import, sorting and assembly.
    Biochim Biophys Acta. 1991 Nov 13;1071(3):221-53 PMID: 1958688
  120. Lipid polymorphism: a correction. The structure of the cubic phase of extinction symbol Fd-- consists of two types of disjointed reverse micelles embedded in a three-dimensional hydrocarbon matrix.
    Biochemistry. 1992 Jan 14;31(1):279-85 PMID: 1731877
  121. Correlation between bilayer lipid dynamics and activity of the diglucosyldiacylglycerol synthase from Acholeplasma laidlawii membranes.
    Biochemistry. 1996 Aug 6;35(31):10094-102 PMID: 8756472
  122. Envelope membrane proteins that interact with chloroplastic precursor proteins.
    Plant Cell. 1994 Jan;6(1):93-105 PMID: 8130644
  123. Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the '16:3' plant Arabidopsis thaliana.
    Biochem J. 1986 Apr 1;235(1):25-31 PMID: 3741384
  124. Comparison of the kinetic properties of MGDG synthase in mixed micelles and in envelope membranes from spinach chloroplast.
    FEBS Lett. 1994 Oct 3;352(3):307-10 PMID: 7925991
  125. Phospholipids as a possible instrument for translocation of nascent proteins across biological membranes.
    Biosci Rep. 1986 Sep;6(9):775-82 PMID: 3028524
  126. A novel chloroplastic outer membrane-targeting signal that functions at both termini of passenger polypeptides.
    J Biol Chem. 1997 Apr 18;272(16):10968-74 PMID: 9099756
  127. Targeting of proteins to the outer envelope membrane uses a different pathway than transport into chloroplasts.
    Plant Cell. 1991 Jul;3(7):709-17 PMID: 1841725
  128. Exchange of protein molecules through connections between higher plant plastids.
    Science. 1997 Jun 27;276(5321):2039-42 PMID: 9197266
  129. Lipid-peptide interactions between fragments of the transit peptide of ribulose-1,5-bisphosphate carboxylase/oxygenase and chloroplast membrane lipids.
    FEBS Lett. 1991 Oct 21;291(2):350-4 PMID: 1936285
  130. Characterization of the import process of a transit peptide into chloroplasts.
    J Biol Chem. 1995 Sep 22;270(38):22368-73 PMID: 7673221
  131. A light-induced protease from barley plastids degrades NADPH:protochlorophyllide oxidoreductase complexed with chlorophyllide.
    Mol Cell Biol. 1995 Nov;15(11):6206-12 PMID: 7565773
  132. Polymorphic regulation of membrane lipid composition.
    Nature. 1987 Oct 15-21;329(6140):587-8 PMID: 3657984
  133. Non-bilayer lipids are required for efficient protein transport across the plasma membrane of Escherichia coli.
    EMBO J. 1995 Nov 15;14 (22):5506-13 PMID: 8521807
  134. Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. II. Biochemical characterization.
    J Biol Chem. 1983 Nov 10;258(21):13281-6 PMID: 6630230
  135. Formation of inverted lipid micelles in aqueous dispersions of mixed sn-3-galactosyldiacylglycerols induced by heat and ethylene glycol.
    Biochim Biophys Acta. 1982 Apr 7;686(2):215-24 PMID: 7082664
  136. In vivo function and membrane binding properties are correlated for Escherichia coli lamB signal peptides.
    Science. 1985 May 31;228(4703):1096-9 PMID: 3158076
  137. Latent membrane perturbation activity of a mitochondrial precursor protein is exposed by unfolding.
    EMBO J. 1988 Apr;7(4):1153-8 PMID: 2841114
Article Info
Journal
Plant molecular biology
Abbr.
Plant Mol Biol
ISSN
0167-4412
Email
[email protected]
Published
1998-09-00
Pages
223-46
Language
English
Region
Netherlands
NLM ID
9106343
Subset
IM
External Links
PubMed source View journal details
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