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Biosynthesis of Thylakoid Membrane Lipids

  • Roland Douce
  • Jacques Joyard
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 4)

Summary

Plastid membranes (thylakoids as well as the two envelope membranes) contain specific polar lipids (galactolipids, sulfolipid, phospholipids), pigments (chlorophylls, carotenoids) and prenylquinones (plastoquinone, tocopherols). In this chapter, we describe our present understanding of the structure of these lipids and their distribution within chloroplasts, of the biosynthetic pathway for glycerolipids, pigments and prenylquinones and of the biochemical properties of the enzymes involved. The biosynthesis of plastid glycerolipids takes place in the inner envelope membrane, which is the site of assembly of fatty acids, glycerol and polar head groups (galactose, for galactolipids; sulfoquinovose, for sulfolipid and glycerol for phosphatidylglycerol). The inner envelope membrane contains all the enzymatic equipment for the biosynthesis of glycerolipids containing almost exclusively a C18/C16 diacylgycerol backbone. In contrast, the origin of plastid glycerolipids with a C18/C18 diacylglycerol backbone is still poorly understood. Then, fatty acids of the newly synthesized molecules are desaturated to form the polyunsaturated molecular species that are characteristic of plastid glycerolipids. Although the sequences of reactions involved in the biosynthesis of plastid prenyllipids (pigments and prenylquinones) have been thoroughly studied, little is known about the precise localization and properties of the different enzymes involved. There is a tight cooperation within chloroplasts between the stroma, the envelope membranes and the thylakoids to form the various pigments (chlorophyll and carotenoids) and prenylquinones (plastoquinone-9 and α-tocopherol), and many of the enzymes involved are in fact located in the inner envelope membrane. Because thylakoids represent the main proportion of the plastid membranes, they contain the largest amount of the plastid lipid constituents, therefore massive transport of lipid molecules from their site of synthesis (envelope membranes) to their site of accumulation (thylakoids) should take place during plastid development. The possible mechanisms that could be involved, i.e. vesicular transport, transfer of lipid monomers through the stroma either by facilitated transport or by spontaneous diffusion of free monomers, lateral diffusion of lipids between membranes at regions of direct intermembrane contact, will be discussed.

Abbreviations

ACP – acyl carrier protein DAG – diacylglycerol DGDG – digalactosyldiacylglycerol LHC – light-harvesting complex MGDG – monogalactosyldiacylglycerol PA – phosphatidic acid PC – phosphatidylcholine PG – phosphatidyl-glycerol SL – sulfolipid SQ – sulfoquinovose SQDG – sulfoquinovosyldiacylglycerol 

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References

  1. Alban C, Dorne AJ, Joyard J and Douce R (1989a) [14C]-acetate incorporation into glycerolipids from cauliflower proplastids and sycamore amyloplasts. FEBS Lett 249: 95–99CrossRefGoogle Scholar
  2. Alban C, Joyard J and Douce R (1989b) Comparison of glycerolipid biosynthesis in non-green plastids from sycamore (Acer pseudoplatanus) cells and cauliflower (Brassica oleracea) buds. Biochem J 259: 775–783PubMedGoogle Scholar
  3. Andrews J and Mudd JB (1985) Phosphatidylglycerol synthesis in pea chloroplasts. Pathway and localization. Plant Physiol 79: 259–265PubMedGoogle Scholar
  4. Andrews J, Ohlrogge J and Keegstra K (1985) Final steps of phosphatidic acid synthesis in pea chloroplasts occurs in the inner envelope membrane. Plant Physiol 78: 459–465PubMedGoogle Scholar
  5. Andrews J, Schmidt H and Heinz E (1989) Interference of electron transport inhibitors with desaturation of monogalactosyl diacylglycerol in intact chloroplasts. Arch Biochem Biophys 270: 611–622PubMedCrossRefGoogle Scholar
  6. Armstrong GA, Hundle BS and Hearst JE (1993) Evolutionary conservation and structural similarities of carotenoid biosynthesis gene products from photosynthetic and nonphotosynthetic organisms. Meth Enzymol 214: 297–311PubMedGoogle Scholar
  7. Barry P and Pallett KE (1990) Herbicidal inhibition of carotenogenesis detected by HPLC. Z Naturforsch 45: 492–497Google Scholar
  8. Bartley GE, Viitanen P, Bacot KO and Scolnik PA (1992) A tomato gene expressed during fruit ripening encodes an enzyme of the carotenoid biosynthesis pathway. J Biol Chem 267: 5036–5039PubMedGoogle Scholar
  9. Bartley GE, Kumle A, Beyer P and Scolnik PA (1993) Functional analysis and purification of enzymes for carotenoid biosynthesis expressed in photosynthetic bacteria. Meth Enzymol 214: 374–385PubMedGoogle Scholar
  10. Beale SI (1990) Biosynthesis of the tetrapyrrole pigment precursor, δ-aminolevulinic acid, from glutamate. Plant Physiol 93: 1273–1279PubMedGoogle Scholar
  11. Beale SI and Weinstein JD (1990) Tetrapyrrole metabolism in photosynthetic organisms. In: Dailey HA (ed) Biosynthesis of Heme and Chlorophylls, pp 287–391. McGraw-Hill Publishing Co, New YorkGoogle Scholar
  12. Benli M, Schulz R and Apel K (1991) Effect of light on the NADPH-protochlorophyllide oxidoreductase of Arabidopsis thaliana. Plant Mol Biol 16: 615–625PubMedCrossRefGoogle Scholar
  13. Bertrams M and Heinz E (1981) Positional specificity and fatty acid selectivity of purified sn-glycerol-3-phosphate acyl-transferase from chloroplasts. Plant Physiol 68: 653–657PubMedGoogle Scholar
  14. Bertrams M, Wrage K and Heinz E (1981) Lipid labelling in intact chloroplasts from exogenous nucleotide precursors. Z Naturforsch 36: 62–70Google Scholar
  15. Beyer P (1987) Solubilization and reconstitution of carotenogenic enzymes from daffodil chromoplast membranes using 3-[(3-cholamidopropyl)dimethylammonio]-1-propane sulfonate. Meth Enzymol 148: 392–400Google Scholar
  16. Beyer P and Kleinig H (1990) On the desaturation and cyclization reactions of carotenes in chromoplast membranes. In: Krinsky NI, Mathews-Roth MM and Taylor RF (eds) Carotenoids: Chemistry and Biology, pp 195–206. Plenum Press, New YorkGoogle Scholar
  17. Bickel H and Schultz G (1976) Biosynthesis of plastoquinone and β-carotene in isolated chloroplasts. Phytochem 15: 1253–1255CrossRefGoogle Scholar
  18. Bickel H, Palme L and Schultz G (1978) Incorporation of shikimate and other precursors into aromatic amino acids and prenylquinones of isolated spinach chloroplasts. Phytochem 17: 119–124CrossRefGoogle Scholar
  19. Billecocq A, Douce R and Faure M (1972) Structure des membranes biologiques: Localisation des galactosyl-diglycérides dans les chloroplastes au moyen des anticorps spécifiques. CR Acad Sci Paris 275: 1135–1137Google Scholar
  20. Bishop DG (1986) Chilling sensitivity in higher plants: The role of phosphatidylglycerol. Plant Cell Env 9: 613–616Google Scholar
  21. Bishop DG, Sparace SA and Mudd JB (1985) Biosynthesis of sulfoquinovosyldiacylglycerol in higher plants: The origin of the diacylglycerol moiety. Arch Biochem Biophys 240: 851–858PubMedCrossRefGoogle Scholar
  22. Bishop WR and Bell RM (1988) Assembly of phospholipids into cellular membranes: Biosynthesis, transmembrane movement and intracellular location. Annu Rev Cell Biol 4: 579–610PubMedCrossRefGoogle Scholar
  23. Bligny R, Gardeström P, Roby C and Douce R (1990) 31P NMR studies of spinach leaves and their chloroplasts. J Biol Chem 265: 1319–1326PubMedGoogle Scholar
  24. Block MA, Joyard J and Douce R (1980) Site of synthesis of geranylgeraniol derivatives in intact spinach chloroplasts. Biochim Biophys Acta 631: 210–219PubMedGoogle Scholar
  25. Block MA, Dorne AJ, Joyard J and Douce R (1983a) Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. I–Electrophoretic and immunochemical analyses. J Biol Chem 258: 13273–13280PubMedGoogle Scholar
  26. Block MA, Dorne AJ, Joyard J and Douce R (1983b) Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. II–Biochemical characterization. J Biol Chem 258: 13281–13286PubMedGoogle Scholar
  27. Block MA, Joyard J and Douce R (1992) Purification and characterization of E37, a major envelope protein. FEBS Lett 287: 765–769Google Scholar
  28. Bramley PM (1985) The in vitro biosynthesis of carotenoids. Adv Lip Res 21: 243–279Google Scholar
  29. Britton G (1988) Biosynthesis of carotenoids. In: TW Goodwin (ed) Plant Pigments, pp 133–182. Academic Press, LondonGoogle Scholar
  30. Browse J, McCourt P and Somerville C (1985) A mutant of Arabidopsis lacking a chloroplast-specific lipid. Science 227: 763–765PubMedGoogle Scholar
  31. Buckner B and Robertson DS (1993) Cloning of carotenoid biosynthetic genes from maize. Meth Enzymol 214: 311–323PubMedGoogle Scholar
  32. Buckner B, Kelson TL and Robertson DS (1990) Cloning of the y1 locus of maize, a gene involved in the biosynthesis of carotenoids. Plant Cell 2: 867–876PubMedCrossRefGoogle Scholar
  33. Camara B (1993) Plant phytoene synthase complex: Component enzymes, immunology and biogenesis. Meth Enzymol 214: 352–365.Google Scholar
  34. Camara B, Bardat F, Seye A, D’Harlingue A and Monéger R (1982) Terpenoid metabolism in plastids. Localization of α-tocopherol synthesis in Capsicum chromoplasts. Plant Physiol 70: 1562–1563PubMedGoogle Scholar
  35. Carde JP, Joyard J, Douce R (1982) Electron microscopic studies of envelope membranes from spinach plastids. Biol Cell 44: 315–324Google Scholar
  36. Carman GM and Henry SA (1989) Phospholipid biosynthesis in yeast. Annu Rev Biochem 58: 635–669PubMedCrossRefGoogle Scholar
  37. Carter HE, McCluer RH and Slifer ED (1956) Lipids of wheat flour. I. Characterization of galactosylglycerol components. J Am Chem Soc 78: 3735–3738CrossRefGoogle Scholar
  38. Castelfranco PA and Beale SI (1983) Chlorophyll biosynthesis: Recent advances and areas of current interest. Annu Rev Plant Physiol 34: 241–278CrossRefGoogle Scholar
  39. Castelfranco PA, Rich PM and Beale SI (1974) The abolition of lag phase in greening cucumber cotyledons by exogenous δ-antinolevulinic acid. Plant Physiol 53: 615–618PubMedGoogle Scholar
  40. Cline K, Andrews J, Mersey B, Newcomb EH and Keegstra K (1981) Separation and characterization of inner and outer envelope membranes of pea chloroplasts. Proc Natl Acad Sci USA 78: 3595–3599PubMedGoogle Scholar
  41. Cogdell R (1988) The function of pigments in chloroplasts. In: TW Goodwin (ed) Plant Pigments, pp 183–230. Academic Press, LondonGoogle Scholar
  42. Costes C, Burghoffer C, Joyard J, Block MA and Douce R (1979) Occurrence and biosynthesis of violaxanthin in isolated spinach chloroplast envelope. FEBS Lett 103: 17–21CrossRefGoogle Scholar
  43. Covès J, Block MA, Joyard J and Douce R (1986) Solubilization and partial purification of UDP-galactose:diacylglycerol galactosyltransferase activity from spinach chloroplast envelope. FEBS Lett 208: 401–406Google Scholar
  44. Covès J, Pineau B, Block MA, Joyard J and Douce R (1987) Solubilization and partial purification of chloroplast envelope proteins: Application to UDP-galactose:diacylglycerol galactosyltransferase. In Leaver C and Sze H (eds) Plant Membranes: Structure, Function, Biogenesis, pp 103–112. Alan R. Liss, New YorkGoogle Scholar
  45. Covès J, Joyard J and Douce R (1988) Lipid requirement and kinetic studies of solubilized UDP-galactose:diacylglycerol galactosyltransferase activity from spinach chloroplast envelope membranes. Proc Natl Acad Sci USA 85: 4966–4970PubMedGoogle Scholar
  46. D’Harlingue A and Camara B (1985) Plastid enzymes of terpenoid biosynthesis. Purification and characterization of γ-tocopherol methyltransferase from Capsicum chromoplasts. J Biol Chem 260: 15200–15203Google Scholar
  47. Dahlin D (1993) Import of nuclear-encoded proteins into carotenoid-deficient young etioplasts. Physiol Plant 87: 410–416CrossRefGoogle Scholar
  48. Darrah PM, Kay SA, Teakle GR and Griffiths WT (1990) Cloning and sequencing of protochlorophyllide reductase. Biochem J 265: 789–798PubMedGoogle Scholar
  49. Deems RA, Eaton BR and Dennis EA (1975) Kinetic analysis of phospholipase A2 activity towards mixed micelles and its implication for the study of lipolytic enzymes. J Biol Chem 250: 9013–9020PubMedGoogle Scholar
  50. Dehesh K, van Cleve B, Ryberg M and Apel K (1986) Light-induced changes in the distribution of the 36,000-Mr polypeptide of NADPH-protochlorophyllide oxidoreductase within different compartments of barley (Hordeum vulgare L.) Planta 169: 172–183Google Scholar
  51. Demmig-Adams B and Adams WW III (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43: 599–626CrossRefGoogle Scholar
  52. Deruère J, Römer S, ďHarlingue A, Backhaus RA, Kuntz M and Camara B (1994) Fibril assembly and carotenoid over-accumulation in chromoplasts: A model for supramolecular lipoprotein structures. The Plant Cell 6: 119–133PubMedGoogle Scholar
  53. Dorne A-J and Heinz E (1989) Position and pairing of fatty acids in phosphatidylglycerol from pea leaf chloroplasts and mitochondria. Plant Sci 60: 39–46CrossRefGoogle Scholar
  54. Dorne A-J, Block MA, Joyard J and Douce R (1982) The galactolipid:galactolipid galactosyltransferase is located on the outer membrane of the chloroplast envelope. FEBS Lett 145: 30–34CrossRefGoogle Scholar
  55. Dorne A-J, Joyard J, Block MA and Douce R (1985) Localization of phosphatidylcholine in outer envelope membrane of spinach chloroplasts. J Cell Biol 100: 1690–1697PubMedCrossRefGoogle Scholar
  56. Dorne A-J, Joyard J and Douce, R (1990) Do thylakoids really contain phosphatidylcholine? Proc Natl Acad Sci USA 87: 71–74PubMedGoogle Scholar
  57. Douady D and Dubacq J-P (1987) Purification of acyl-CoA:glycerol-3-phosphate acyltransferase from pea leaves. Biochim Biophys Acta 921: 615–619Google Scholar
  58. Douce R (1974) Site of synthesis of galactolipids in spinach chloroplasts. Science 183: 852–853PubMedGoogle Scholar
  59. Douce R and Joyard J (1980) Plant galactolipids. In: Stumpf PK (ed) The Biochemistry of Plants: Lipids: Structure and Function, Vol 4, pp 321–362. Academic Press, New YorkGoogle Scholar
  60. Elstner EF (1987) Metabolism of activated oxygen species. In: Davies DD (ed) The Biochemistry of Plants: Biochemistry of Metabolism, Vol 11, pp 253–315. Academic Press, New YorkGoogle Scholar
  61. Fiedler E, Soll J and Schultz G (1982) The formation of homogentisate in the biosynthesis of tocopherol and plastoquinone in spinach chloroplasts. Planta 155: 511–515CrossRefGoogle Scholar
  62. Flügee UI and Benz R (1984) Pore-forming activity in the outer membrane of the chloroplast envelope. FEBS Lett 169: 85–89Google Scholar
  63. Frank F and Strzalka K (1992) Detection of the photoactive protochlorophyllide-protein complex in the light during the greening of barley. FEBS Lett 309: 73–77Google Scholar
  64. Frentzen M (1986) Biosynthesis and desaturation of the different diacylglycerol moieties in higher plants. J Plant Physiol 124: 193–209Google Scholar
  65. Frentzen M (1993) Acyltransferases and triacylglycerol. In: Moore ST Jr (ed) Lipid Metabolism in Plants, pp 195–230. CRC Press, Boca RatonGoogle Scholar
  66. Frentzen M, Heinz E, McKeon TA and Stumpf PK (1983) Specificities and selectivities of glycerol-3-phosphate acyltransferase and monoacylglycerol-3-phosphate acyltransferase from pea and spinach chloroplasts. Eur J Biochem 129: 629–636PubMedGoogle Scholar
  67. Fuesler TP, Wong YS and Castelfranco PA (1984) Localization of Mg-chelatase and Mg-protoporphyrin IX monomethyl ester (oxidative) cyclase activities within isolated, developing cucumber cotyledons. Plant Physiol 75: 662–664PubMedGoogle Scholar
  68. Garnier J, Wu B, Maroc J, Guyon D and Trémolières A (1990) Restoration of both an oligomeric form of the light-harvesting antenna CPII and a fluorescence state II-state I transition by D3-trans-hexadecenoic acid-containingphosphatidylglycerol, in cells of a mutant of Chlamydomonas reinhardtii. Biochim Biophys Acta 1020: 153–162Google Scholar
  69. Goodwin TW (1993) Biosynthesis of carotenoids: An overview. Meth Enzymol 214: 330–340Google Scholar
  70. Goodwin TW and Britton G (1988) Distribution and analysis of carotenoids. In: TW Goodwin (ed) Plant Pigments, pp 61–132. Academic Press, LondonGoogle Scholar
  71. Gounaris, K. and Barber, J.(1983) Monogalactosyldiacylglycerol: The most abundant polar lipid in Nature. Trends Biochem Sci 9: 378–381Google Scholar
  72. Gray JC (1987) Control of isoprenoid biosynthesis in higher plants. Adv Bot Res 14: 25–91Google Scholar
  73. Grevby C, Engdahl,, Ryberg M and Sundqvist C (1989) Binding properties of NADPH-protochlorophyllide oxidoreductase as revealed by detergent and ion treatments of isolated and immobilized prolamellar bodies, Physiol Plant 77: 493–503Google Scholar
  74. Gunning BES and Steer MW (1975) Ultrastructure and the Biology of Plant Cell, Edward Arnold: LondonGoogle Scholar
  75. Haas R, Siebertz HP, Wrage K and Heinz E (1980) Localization of sulfolipid labeling within cells and chloroplasts. Planta 148: 238–244CrossRefGoogle Scholar
  76. Haverkate F and Van Deenen LLM (1965) Isolation and chemical characterization of phosphatidylglycerol from spinach leaves. Biochim Biophys Acta 106: 78–92PubMedGoogle Scholar
  77. Heber U and Heldt HW (1981) The chloroplast envelope: Structure, function, and role in leaf metabolism. Ann Rev Plant Physiol 32: 139–168Google Scholar
  78. Heemskerk JWM and Wintermans JFGM (1987) The role of the chloroplast in the leaf acyl-lipid synthesis. Physiol Plant 70: 558–68Google Scholar
  79. Heemskerk JHW, Storz T, Schmidt RR and Heinz E (1990) Biosynthesis of digalactolsyldiacylglycerol in plastids from 16∶3 and 18∶3 plants. Plant Physiol 93: 1286–1294PubMedGoogle Scholar
  80. Heinz E (1977) Enzymatic reactions in galactolipid biosynthesis. In: Tevini M and Licthenthaler HK (eds) Lipids and Lipid Polymers, pp 102–120. Springer Verlag, BerlinGoogle Scholar
  81. Heinz E (1993) Biosynthesis of polyunsaturated fatty acids. In: Moore ST Jr (ed) Lipid Metabolism in Plants, pp 34–89. CRC Press, Boca RatonGoogle Scholar
  82. Heinz E and Roughan PG (1983) Similarities and differences in lipid metabolism of chloroplasts isolated from 18∶3 and 16∶3 plants. Plant Physiol 72: 273–279PubMedCrossRefGoogle Scholar
  83. Heinz E, Schmidt H, Hoch M, Jung K-H, Binder H and Schmidt RR (1989) Synthesis of different nucleoside 5′-diphospho-sulfoquinovoses and their use for studies on sulfolipid biosynthesis in chloroplasts. Eur J Biochem 184: 445–453PubMedCrossRefGoogle Scholar
  84. Herrin DL, Battey JF, Greer K and Schmidt GW (1992) Regulation of chlorophyll apoprotein expression and accumulation: Requirements for carotenoids and chlorophyll. J Biol Chem 267: 8260–8269PubMedGoogle Scholar
  85. Hinterstoisser B, Missbichler A, Pineau B and Peschek G (1988) Detection of chlorophyllide in chlorophyll-free plasma membrane preparations from Anacystis nidulans. Biochem Biophys Res Comm 154: 839–846PubMedCrossRefGoogle Scholar
  86. Hobe S, Prytulla S, Külbrandt W and Paulsen H (1994) Trimerization and crystallization of reconstituted light-harvesting chlorophyll a/b complex. EMBO J 13: 3423–3429PubMedGoogle Scholar
  87. Hugueney P, Römer S, Kuntz M and Camara B (1992) Characterization and molecular cloning of a bifunctional flavoprotein catalyzing the synthesis of phytofluene and zeta-carotene in Capsicum chromoplasts. Eur J Biochem 209:399–407PubMedCrossRefGoogle Scholar
  88. Humbeck K, Römer S and Senger H (1989) Evidence for an essential role of carotenoids in the assembly of an active photosystem II. Planta 179: 242–250CrossRefGoogle Scholar
  89. Hutson KG and Threlfall DR (1980) Synthesis of plastoquinone-9 and phytylplastoquinone from homogentisate in lettuce chloroplasts. Biochim Biophys Acta 632: 630–648PubMedGoogle Scholar
  90. Ikeuchi M and Murakami S (1982) Behavior of the 36,000-dalton protein in the internal membranes of squash etioplasts during greening. Plant Cell Physiol 23: 575–583Google Scholar
  91. Ilag LL, Kumar AM and Söll D (1994) Light regulation of chlorophyll biosynthesis at the level of aminolevulinate formation in Arabidopsis. Plant Cell 6: 265–275PubMedCrossRefGoogle Scholar
  92. Ishiko H, Shigeoka S, Nakano Y and Mitsunaga T (1992) Some properties of γ-tocopherol methyltransferase solubilized from spinach chloroplasts Phytochem 31: 1499–1500CrossRefGoogle Scholar
  93. Ishizaki O, Nishida I, Agata K, Eguchi G and Murata N (1988) Cloning and nucleotide sequence of cDNA for the plastid glycerol-3-phosphate acyltransferase from squash. FEBS Lett 238: 424–430PubMedCrossRefGoogle Scholar
  94. Jeffrey SW, Douce R and Benson AA (1974) The carotenoids of the chloroplast envelope. Proc Natl Acad Sci USA 71: 807–810PubMedGoogle Scholar
  95. Johanningmeier U and Howell SH (1984) Regulation of light-harvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardtii. Possible involvement of chlorophyll synthesis precursors. J Biol Chem 259: 13541–13549PubMedGoogle Scholar
  96. Jones BL and Porter JW (1986) Biosynthesis of carotenes in higher plants. CRC Crit Rev Plant Sci 3: 295–324Google Scholar
  97. Jones OTG (1968) Ferrochelatase of spinach chloroplasts. Biochem J 107: 113–119PubMedGoogle Scholar
  98. Joyard J and Douce R (1976a) Ľenveloppe des chloroplastes estelle capable de synthétiser la phosphatidylcholine? CR Acad Sci Paris 282: 1515–1518Google Scholar
  99. Joyard J and Douce R (1976b) Mise en évidence et rôle des diacylglycérols dans ľenveloppe des chloroplastes d’épinard. Biochim Biophys Acta 424: 126–131Google Scholar
  100. Joyard J and Douce R (1977) Site of synthesis of phosphatidic acid and diacylglycerol in spinach chloroplasts. Biochim Biophys Acta 486: 273–285PubMedGoogle Scholar
  101. Joyard J and Douce R (1979) Characterization of phosphatidate phosphohydrolase activity associated with chloroplast envelope membranes. FEBS Lett 102: 147–150PubMedCrossRefGoogle Scholar
  102. Joyard J and Douce R (1987) Galactolipid biosynthesis. In: Stumpf PK (ed) The Biochemistry of Plants: Lipids: Structure and Function, Vol 9, pp 215–274. Academic Press, New YorkGoogle Scholar
  103. Joyard J, Douce R, Siebertz HP and Heinz E (1980) Distribution of radioactive lipids between envelopes and thylakoids from in vivo labeled chloroplasts. Eur J Biochem 108: 171–176PubMedCrossRefGoogle Scholar
  104. Joyard J, Blée E and Douce R (1986) Sulfolipid synthesis from 35SO4 2 and [1-14C]-acetate in isolated intact spinach chloroplasts. Biochim Biophys Acta 879: 78–87Google Scholar
  105. Joyard J, Block MA, Pineau B, Albrieux C and Douce R (1990) Envelope membranes from mature spinach chloroplasts contain a N ADPH: protochlorophyllide reductase on the cytosolic side of the outer membrane. J Biol Chem 265: 21820–21827PubMedGoogle Scholar
  106. Joyard J, Block MA and Douce R (1991) Molecular aspects of plastid envelope biochemistry. Eur J Biochem 199: 489–509PubMedCrossRefGoogle Scholar
  107. Joyard J, Block MA, Malherbe A, Maréchal E and Douce R (1993) Origin and synthesis of galactolipid and sulfolipid head groups. In: Moore ST Jr (ed) Lipid Metabolism in Plants, pp 231–258. CRC Press, Boca RatonGoogle Scholar
  108. Kader JC (1990) Intracellular transfer of phospholipids, galactolipids and fatty acids in plant cells. Subcell Biochem 16: 69–111PubMedGoogle Scholar
  109. Kader JC (1993) Lipid transport in plants. In: Moore ST Jr (ed) Lipid Metabolism in Plants, pp 309–336. CRC Press, Boca RatonGoogle Scholar
  110. Keegstra K, Olsen LJ and Theg SM (1989) Chloroplastic precursors and their transport across the envelope membranes. Ann Rev Plant Physiol Plant Mol Biol 40: 471–501CrossRefGoogle Scholar
  111. Klein RR and Mullet JE (1987) Control of gene expression during higher plant chloroplast biogenesis. Protein synthesis and transcript levels of psbA, psaA-psaB, and rbcL in dark-grown and illuminated barley seedlings. J Biol Chem 262: 4341–4348PubMedGoogle Scholar
  112. Kleinig H (1989) The role of plastids in isoprenoid biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40: 39–59CrossRefGoogle Scholar
  113. Kleppinger-Sparace KF, Mudd JB and Bishop DG (1985) Biosynthesis of sulfoquinovosyldiacylglycerol in higher plants: The incorporation of 35SO4 by intact chloroplasts. Arch Biochem Biophys 240: 859–865PubMedGoogle Scholar
  114. Kunst L, Browse J and Sommerville 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: 4143–4147PubMedGoogle Scholar
  115. Kuntz M, Römer S, Suire C, Hugueney P, Weil JH, Schantz R and Camara B (1992) Identification of a cDNA for the plastid located geranylgeranyl pyrophosphate synthase from Capsicum annuum: Correlative increase in enzyme activity and transcript level during fruit ripening. Plant J 21: 25–34Google Scholar
  116. Lawlor DW (1987) Photosynthesis: Metabolism, Control and Physiology. Longman Scientific and Technical, Harlow, UK.Google Scholar
  117. Li HM, Moore T and Keegstra K (1991) Targeting of proteins to the outer envelope membrane uses a different pathway than transport into chloroplasts. Plant Cell 3: 709–717PubMedGoogle Scholar
  118. Lichtenthaler HK (1993) The plant prenyllipids, including carotenoids, chlorophylls, and prenylquinones. In: Moore ST Jr (ed) Lipid Metabolism in Plants, pp 427–470. CRC Press, Boca RatonGoogle Scholar
  119. Lichtenthaler HK, Prenzel H, Douce R and Joyard J (1981) Localization of prenylquinones in the envelope of spinach chloroplasts. Biochim Biophys Acta 641: 99–105PubMedGoogle Scholar
  120. Lindblom G and Rilfors L (1989) Cubic phases and isotropic structures formed by membrane lipids. Possible biological relevance. Biochim Biophys Acta 988: 221–256Google Scholar
  121. Lütke-Brinkhaus F, Liedvogel B, Kreuz K and Kleinig H (1982) Phytoene synthase and phytoene dehydrogenase associated with envelope membranes from spinach chloroplasts. Planta 156: 176–180Google Scholar
  122. Lützow M and Kleinig H (1990) Chlorophyll-free chromoplasts from daffodil contain most of the enzymes for chlorophyll synthesis in a highly active form. Arch Biochem Biophys 277: 94–100PubMedGoogle Scholar
  123. Malherbe A, Block MA, Joyard J and Douce R (1992) Feedback inhibition of phosphatidate phosphatase from spinach chloroplast envelope membranes by diacylglycerol. J Biol Chem 267: 23546–23553PubMedGoogle Scholar
  124. Malherbe A, Block MA, Douce R and Joyard J (1995) Solubilization and biochemical properties of phosphatidate phosphatase from spinach chloroplast envelope membranes. Plant Physiol Biochem 33: 149–161Google Scholar
  125. Maréchal E, Block MA, Joyard J and Douce R (1991) Purification de ľUDP-galactose: 1,2-diacylglycérol galactosyltransferase de ľ‘enveloppe des chloroplastes d’épinard. C R Acad Sci Paris 313: 521–528Google Scholar
  126. Maréchal E, Block MA, Joyard J and Douce R (1994a) Kinetic properties of monogalactosyldiacylglycerol synthase from spinach chloroplast envelope membranes. J Biol Chem 269: 5788–5798PubMedGoogle Scholar
  127. Maréchal E, Block MA, Joyard J and Douce R (1994b) Comparison of the kinetic properties of MGDG synthase in mixed micelles and in envelope membranes from spinach chloroplast. FEBS Lett 352: 307–310PubMedGoogle Scholar
  128. Maréchal E, Miége C, Block MA, Douce R and Joyard J (1995) The catalytic site of monogalactosyldiacylglycerol synthase from spinach chloroplast envelope membranes. Biochemical analysis of the structure and of the metal content. J Biol Chem 270: 5714–5722PubMedGoogle Scholar
  129. Markwell J, Bruce BD and Keegstra K (1992) Isolation of a carotenoid-containing submembrane particle from the chloroplastic envelope outer membrane of pea (Pisum sativum). J Biol Chem 267: 13933–13937PubMedGoogle Scholar
  130. Martin BA and Wilson RF (1984) Subcellular localization of triacylglycerol biosynthesis in spinach leaves. Lipids 19: 117–121Google Scholar
  131. Matringe M, Camadro JM, Block MA, Joyard J, Scalla R, Labbe P and Douce R (1992) Localization within chloroplasts of protoporphyrinogen oxidase, the target enzyme for diphenyl-ether-like herbicides. J Biol Chem 267: 4646–4651PubMedGoogle Scholar
  132. Matringe M, Camadro JM, Joyard J and Douce R (1994) Localization of ferrochelatase activity within mature pea chloroplasts. J Biol Chem 269: 15010–15015PubMedGoogle Scholar
  133. Mayer H and Isler O (1971) Synthesis of vitamin E. Meth Enzymol 18C: 241–248Google Scholar
  134. Mayer MP, Beyer P and Kleinig H (1990) Quinone compounds are able to replace molecular oxygen as terminal electron acceptor in phytoene desaturation in chromoplasts of Narcissus pseudonarcissus L. Eur J Biochem 191: 359–363PubMedCrossRefGoogle Scholar
  135. Miquel M, Block MA, Joyard J, Dorne A-J, Dubacq J-P, Kader J-C and Douce R (1987) Protein-mediated transfer of phosphatidylcholine from liposomes to spinach chloroplast envelope membranes. Biochim Biophys Acta 937: 219–228Google Scholar
  136. Morelli G, Neslon MA, Ballario P and Macino G (1993) Photoregulated carotenoid biosynthetic genes of Neurospora crassa. Meth Enzymol 214: 412–24PubMedGoogle Scholar
  137. Morré DJ, Morré JT, Morré SR, Sundqvist C and Sandelius AS (1991) Chloroplast biogenesis. Cell-free transfer of envelope monogalactosylglycerides to thylakoids. Biochim Biophys Acta 1070: 437–445PubMedGoogle Scholar
  138. Morris SR and Threlfall DR (1983) Synthesis of 2-methyl-6-phytyl-1,4-benzoquinone by a membrane preparation of the cyanobacterium Anabaena variabilis. Biochem Soc trans 11: 587–588Google Scholar
  139. Mudd JB and de Zacks R (1981) Synthesis of phosphatidylglycerol by chloroplasts from leaves of Spinacia oleracea L. Arch Biochem Biophys 209: 584–591PubMedCrossRefGoogle Scholar
  140. Mullet JE, Klein PG and Klein RR (1990) Chlorophyll regulates accumulation of the plastid-encoded chlorophyll apoproteins CP43 and D1 by increasing apoprotein stability. Proc Natl Acad Sci USA 87: 4038–4042PubMedGoogle Scholar
  141. Murata N, Sato N, Takahashi N and Hamazaki Y (1982) Compositions and positional distribution of fatty acids in phospholipids from leaves of chilling-sensitive and chilling resistant plants. Plant Cell Physiol 23: 1071–1079Google Scholar
  142. Neuburger M, Joyard J and Douce R (1977) Strong binding of cytochrome c on the envelope of spinach chloroplasts. Plant Physiol 59: 1178–1181PubMedGoogle Scholar
  143. Nishida I and Yamada M (1986) Semisynthesis of a spin-labeled monogalactosyl-diacylglycerol and its application in the assay for galactolipid transfer activity in spinach leaves. Biochim Biophys Acta 813: 298–306Google Scholar
  144. Nishida I, Frentzen M, Ishizaki O and Murata N (1987) Purification of isomeric forms of acyl-[acyl-carrier-protein]:glycerol-3-phosphate acyltransferase from greening squash cotyledons. Plant Cell Physiol 28: 1071–1079Google Scholar
  145. Norman HA, Pillai P and St John JB (1991) In vitro desaturation of monogalactosyldiacylglycerol and phosphatidylcholine molecular species by chloroplast homogenates. Phytochem 30: 2217–2222CrossRefGoogle Scholar
  146. Nussberger S, Dörr K, Wang DN and Külbrandt W (1993) Lipid-protein interactions in crystals of plant light-harvesting complex, J Mol Biol 234: 347–356PubMedGoogle Scholar
  147. Pascal N, Block MA, Pallett K.E, Joyard J and Douce R (1995) Inhibition of carotenoid biosynthesis in sycamore cells deprived of iron. Plant Physiol Biochem 33: 97–104Google Scholar
  148. Pennock JF (1983) The biosynthesis of chloroplastic terpenoid quinones and chromanols. Biochem Soc trans 11: 504–510PubMedGoogle Scholar
  149. Peschek G, Hinterstoisser B, Wastyn M, Kuntner O, Pineau B, Missbichler A and Lang J (1989) Chlorophyll precursors in the plasma membrane of a cyanobacterium, Anacystis nidulans. Characterization of protochlorophyllide and chlorophyllide by spectrophotometry, spectrofluorimetry, solvent partition and high performance liquid chromatography. J Biol Chem 264: 11827–11832PubMedGoogle Scholar
  150. Pineau B, Dubertret G, Joyard J and Douce R (1986) Fluorescence properties of the envelope membranes from spinach chloroplasts. Detection of protochlorophyllide. J Biol Chem 261: 9210–9215PubMedGoogle Scholar
  151. Pineau B, Gérard-Hirne C, Douce R and Joyard J (1993) Identification of the main species of tetrapyrrolic pigments in envelope membranes from spinach chloroplasts. Plant Physiol 102: 821–828PubMedGoogle Scholar
  152. Plumley FG and Schmidt GW (1987) Reconstitution of chlorophyll a/b light-harvesting complexes: Xanthophyll-dependent assembly and energy transfer. Proc Natl Acad Sci USA 84: 146–150PubMedGoogle Scholar
  153. Quinn PJ and Williams WP (1983) The structural role of lipids in photosynthetic membranes. Biochim Biophys Acta 737: 223–266Google Scholar
  154. Rau W (1988) Functions of carotenoids other than in photosynthesis. In: TW Goodwin (ed) Plant Pigments, pp 231–255. Academic Press, LondonGoogle Scholar
  155. Rawyler A, Meylan M and Siegenthaler PA (1991) Galactolipid export from envelope to thylakoid membranes in intact chloroplasts. I. Characterization and involvement in thylakoid asymmetry. Biochim Biophys Acta 1104: 331–341Google Scholar
  156. Rawyler A, Meylan M and Siegenthaler PA (1994) (Galacto)lipid export from envelope to thylakoid membranes in intact chloroplasts. II. A general process with a key role for the envelope in the establishment of lipid asymmetry in thylakoid membranes. Biochim Biophys Acta 1233: 123–133Google Scholar
  157. Roughan PG (1986) Acyl lipid synthesis by chloroplasts isolated from the chilling-sensitive plant Amaranthus lividus L. Biochim Biophys Acta 878: 371–379Google Scholar
  158. Roughan PG and Slack CR (1977) Long-chain acyl-coenzyme A synthetase activity of spinach chloroplasts is concentrated in the envelope. Biochem J 162: 457–459PubMedGoogle Scholar
  159. Roughan PG and Slack CR (1982) Cellular organization of glycerolipid metabolism. Annu Rev Plant Physiol 33: 97–132CrossRefGoogle Scholar
  160. Roughan PG, Mudd JB, McManus TT and Slack CR (1979) Linoleate and α-linolenate synthesis by isolated spinach (Spinacia oleracea) chloroplasts. Biochem J 184: 571–574PubMedGoogle Scholar
  161. Rüdiger W and Schoch S (1988) Chlorophylls. In: TW Goodwin (ed) Plant Pigments, pp 1–59. Academic Press, LondonGoogle Scholar
  162. Ruzicka L (1953) The isoprene rule and the biogenesis of terpenic compounds. Experientia 9: 357–396PubMedCrossRefGoogle Scholar
  163. Sakaki T, Kondo N and Yamada M (1990) Pathway for the synthesis of triacylglycerol from monogalactosyldiacyl-glycerols in ozone-fumigated spinach leaves. Plant Physiol 94:773–780Google Scholar
  164. Salomon M, Fisher K, Flügge UI and Soll J (1990) Sequence analysis and protein import studies of an outer chloroplast envelope polypeptide. Proc Natl Acad Sci USA 87: 5778–5782PubMedGoogle Scholar
  165. Sandmann G (1993) Carotenoid analysis in mutants from Escherichia coli transformed with carotenogenic gene cluster and Scenedesmus obliquus mutant C-6D. Meth Enzymol 214: 341–347PubMedGoogle Scholar
  166. Sastry PS and Kates M (1964) Lipid components of leaves. V. Galactolipids, cerebrosides, and lecithin ofrunner-beanleaves. Biochemistry 3: 1271–1280PubMedGoogle Scholar
  167. Schmidt A, Sandmann G, Armstrong GA, Hearst JE and Böger P (1989) Immunological detection of phytoene desaturase in algae and higher plants using an antiserum raised against a bacterial fusion-gene construct. Eur J Biochem 184: 375–378PubMedCrossRefGoogle Scholar
  168. Schmidt H and Heinz E (1990a) Involvement of ferredoxin in desaturation of lipid-bound oleate in chloroplasts. Plant Physiol 94: 214–220PubMedGoogle Scholar
  169. Schmidt H and Heinz E (1990b) Desaturation of oleoyl groups in envelope membranes from spinach chloroplasts. Proc Natl Acad Sci USA 87: 9477–9480PubMedGoogle Scholar
  170. Schmidt H and Heinz E (1992) n-6 desaturase from chloroplast envelopes: Purification and enzymatic characteristics. In: Cherif A, Miled-Daoud DB, Marzouk B, Smaoui A and Zarrouk M (eds) Metabolism, Structure and Utilization of Plant Lipids, pp 140–143. Cent Natl Ped Tunis, TunisiaGoogle Scholar
  171. Schulz A, Ort O, Beyer P and Kleinig H (1993) SC-0051, a 2-benzoyl-cyclohexane-1,3-dione bleaching herbicide, is a potent inhibitor of the enzyme p-hydroxyphenylpyruvate dioxygenase. FEBS Lett 318: 162–166PubMedCrossRefGoogle Scholar
  172. Schulz R, Steinmüller K, Klaas M, Forreiter C, Rasmussen S, Hiller C and Apel K (1989) Nucleotide sequence of a cDNA coding for the NADPH-protochlorophyllide oxidoreductase (PCR) of barley (Hordeum vulgare L.) and its expression in Escherichia coli. Mol Gen Genet 217: 355–361PubMedGoogle Scholar
  173. Schulze-Siebert D, Homeyer U, Soll J and Schultz G (1987) Synthesis of plastoquinone-9, α-tocopherol and phylloquinone (vitamine Kl) and its integration in chloroplast carbon metabolism of higher plants. In: Stumpf PK, Mudd JB and Nes WD (eds) The Metabolism, Structure, and Function of Plant Lipids, pp 29–36. Plenum Publishing Co, New YorkGoogle Scholar
  174. Seifert U and Heinz E (1992) Enzymatic characteristics of UDP-sulfoquinovose: diacylglycerol sulfoquinovosyltransferase from chloroplast envelopes. Botanica Acta 105: 197–205Google Scholar
  175. Selstam E, Widell A and Johannson BA (1987) A comparison of prolamellar bodies of wheat, Scots pine and Jeffrey pine. Pigment spectra and properties of protochlorophyllide reductase. Physiol Plant 70: 209–214Google Scholar
  176. Shaw P, Henwood J, Oliver R and Griffiths T (1985) Immunogold localization of protochlorophyllide reductase in barley etioplasts. Eur J Cell Biol 39: 50–55Google Scholar
  177. Shigeoka S, Ishiko H, Nakano Y and Mitsunaga T (1992) Isolation and properties of γ-tocopherol methyltransferase in Euglena gracilis. Biochim Biophys Acta 1128: 220–226PubMedGoogle Scholar
  178. Siebertz HP, Heinz E, Linscheid M Joyard J and Douce R (1979) Characterization of lipids from chloroplast envelopes. Eur J Biochem 101: 429–438PubMedCrossRefGoogle Scholar
  179. Siefermann-Harms D (1977) The xanthophyll cycle in higher plants. In: Tevini M and Lichtenthaler HK (eds) Lipids and Lipid Polymers, pp 218–230. Springer Verlag, BerlinGoogle Scholar
  180. Siefermann-Harms D (1985) Carotenoids in photosynthesis. I. Location in photosynthetic membranes and light harvesting functions. Biochim Biophys Acta 811: 325–355Google Scholar
  181. Siefermann-Harms D, Joyard J and Douce R (1978) Lightinduced changes of the carotenoid levels in chloroplast envelopes. Plant Physiol 61: 530–533PubMedGoogle Scholar
  182. Slabas AR and Fawcett T (1992) The biochemistry and molecular biology of plant lipid biosynthesis. Plant Mol Biol 19: 169–191PubMedCrossRefGoogle Scholar
  183. Smeekens S, Weisbeek P and Robinson C (1990) Protein transport into and within chloroplasts. Trends Biochem Sci 15: 73–76PubMedCrossRefGoogle Scholar
  184. Smith BB and Rebeiz CA (1979) Chloroplast biogenesis. XXIV. Intrachloroplastic localization of the biosynthesis and accumulation of protoporphyrin IX, magnesium-proto-porphyrin monoester, and longer wavelength metalloporphyrins during greening. Plant Physiol 63: 227–231PubMedGoogle Scholar
  185. Soler E, Clastre M, Bantignies B, Marigo G and Ambid C (1993) Uptake of isopentenyl diphosphate by plastids isolated from Vitis vitifera L. cell suspensions. Planta 191: 324–329CrossRefGoogle Scholar
  186. Soll J (1987) α-tocopherol and plastoquinone biosynthesis in chloroplast membranes. Meth Enzymol 148: 383–392Google Scholar
  187. Soll J and Alefsen H (1993) The protein import apparatus of chloroplasts. Physiol Plant 87: 433–40Google Scholar
  188. Soll J and Schultz G (1981) Phytol synthesis from geranylgeraniol in spinach chloroplasts. Biochem Biophys Res Commun 99: 907–912PubMedCrossRefGoogle Scholar
  189. Soll J, Douce R and Schultz G (1980a) Site of biosynthesis of atocopherol in spinach chloroplasts. FEBS Lett 112: 243–246CrossRefGoogle Scholar
  190. Soll J, Kemmerling M and Schultz G (1980b) Tocopherol and plastoquinone synthesis in spinach chloroplasts subfractions. Arch Biochem Biophys 204: 544–550PubMedCrossRefGoogle Scholar
  191. Soll J, Schultz G, Rüdiger W and Benz J (1983) Hydrogenation of geranylgeraniol. Two pathways exist in spinach chloroplasts. Physiol Plant 71: 849–854Google Scholar
  192. Soll J, Schultz G, Joyard J, Douce R and Block MA (1985) Localization and synthesis of prenylquinones in isolated outer and inner envelope membranes from spinach chloroplasts. Arch Biochem Biophys 238: 290–299PubMedCrossRefGoogle Scholar
  193. Somerville C and Browse J (1991) Plant lipids: Metabolism, mutants, and membranes. Science 252: 80–87PubMedGoogle Scholar
  194. Spano AJ, He Z and Timko MP (1992a) NADPH:protochlorophyllide oxidoreductases in white pine (Pinus strobus) and loblolly pine (P. taeda). Mol Gen Genet 236: 86–95PubMedGoogle Scholar
  195. Spano AJ, He Z, Michel H, Hunt DF and Timko MP (1992b) Molecular cloning, nuclear gene structure, and developmental expression of NADPH:protochlorophyllide oxidoreductase in pea (Pisum sativum L.). Plant Mol Biol 18: 967–972PubMedCrossRefGoogle Scholar
  196. Stymne S and Stobart AK (1987) Triacylglycerol biosynthesis. In: Stumpf PK (ed) The Biochemistry of Plants: Lipids: Structure and Function, Vol 9, pp 175–214. Academic Press, New YorkGoogle Scholar
  197. Swiezewska E, Dallner G, Andersson B and Ernster L (1993) Biosynthesis of ubiquinone and plastoquinone in the endoplasmic reticulum-Golgi membranes of spinach leaves. J Biol Chem 268: 1494–1499PubMedGoogle Scholar
  198. Taylor WC (1989) Regulatory interactions between nuclear and plastid genomes. Annu Rev Plant Physiol Plant Mol Biol 40: 211–233CrossRefGoogle Scholar
  199. Teakle GR and Griffiths, WT (1993) Cloning, characterization and import studies on protochlorophyllide reductase from wheat (Triticum aestivum). Biochem J 296: 225–230PubMedGoogle Scholar
  200. Teucher T and Heinz E (1991) Purification of UDP-galactose: diacylglycerol from chloroplast envelopes of spinach (Spinacia oleracea L.). Planta 184: 319–326CrossRefGoogle Scholar
  201. Trémolières A, Roche O, Dubertret G, Maroc J, Guyon D and Garnier J (1991) Restoration of thylakoid appression by D3. trans-hexadecenote acid-containing phosphatidylglycerol, in a mutant of Chlamydomonas reinhardtii. Relationship with the regulation of excitation energy distribution. Biochim Biophys Acta 1059: 286–292Google Scholar
  202. Van Besouw A and Wintermans JFGM (1978) Galactolipid formation in chloroplast envelopes. I. Evidence for two mechanisms in galactosylation. Biochim Biophys Acta 529: 44–53PubMedGoogle Scholar
  203. Van Besouw A and Wintermans JFGM (1979) The synthesis of galactolipids by chloroplast envelopes. FEBS Lett 102: 33–37PubMedCrossRefGoogle Scholar
  204. Walker CJ and Weinstein JD (1991 a) Further characterization of the magnesium chelatase in isolated developing cucumber chloroplasts. Plant Physiol 95: 1189–1196PubMedCrossRefGoogle Scholar
  205. Walker CJ and Weinstein JD (1991b) In vitro assay of the chlorophyll biosynthetic enzyme Mg-chelatase: Resolution of the activity into soluble and membrane-bound fractions. Proc Natl Acad Sci USA 88: 5789–5793PubMedGoogle Scholar
  206. Weber S, Wolter FP, Buck F, Frentzen M and Heinz E (1991) Purification and cDNA sequencing of an oleate-selective acyl-ACP:sn-glycerol-3-phosphate acyltransferase from pea chloroplasts. Plant Mol Biol 17: 1067–1076PubMedCrossRefGoogle Scholar
  207. Wellburn AR (1982) Bioenergetic and ultrastructural changes associated with chloroplast development. Int Rev Cytol 80: 133–191Google Scholar
  208. Wrisher M (1989) Ultrastructural localization of photosynthetic activity in thylakoids during chloroplast development in maize. Planta l77: 18–23Google Scholar

Copyright information

© Kluwer Academic Publishers 1996

Authors and Affiliations

  • Roland Douce
    • 1
  • Jacques Joyard
    • 1
  1. 1.Laboratoire de Physiologie Cellulaire Végétale, URA CNRS nº576, Département de Biologie Moléculaire et StructuraleCEA-Centre ďEtudes Nucléaires de Grenoble et Université Joseph FourierGrenoble-cedex 9France

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