Origin of the Plastid Envelope Membranes

  • Roland Douce
  • Jacques Joyard
  • Albert-Jean Dorne
  • Maryse A. Block
Part of the NATO ASI Series book series (NSSA, volume 91)

Abstract

The endosymbiotic theory, first proposed by Schimper (1885) and Mereschkovsky (1905), postulates that the plastids in eukaryotic cells originated as free-living prokaryotes which found shelter within primitive cells (protoeukaryotes) and then became permanent symbiotic elements within them, probably by providing more efficient energy-transducing systems. This suggestion is supported by numerous biochemical studies which favor the evolutionnary relationship between plastids and blue-green algae (see for instance Fredrick, 1981; Schiff, 1982, Whatley, 1983). However, most of the studies done in order to prove the endosymbiotic theory generally focus on the structure and function of DNA and RNA, consider also the major functions (photosynthesis, respiration), but generally pay little attention to an important structural feature of the cell organelles and free-living prokaryotes, i.e. their limiting membranes. Cell organelles, such as all kind of plastids, and some prokaryotes (see Stanier and Cohen-Bazire, 1977), such as gram-negative bacteria and especially blue green algae (cyanobacteria) are limited by a double membrane system. However, it is generally assumed, without experimental evidences, that the inner envelope membrane from chloroplasts could derive from the plasma membrane of the prokaryotic ancestor whereas the outer envelope membrane of chloroplasts could derive from the endomembrane system of the protoeukaryote that engulfed the free living prokaryote.

Keywords

Photosynthesis Flavonoid Cytosol Carotenoid Mannitol 

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References

  1. Allen, C.F., Hirayama, O., and Good, P., 1966, Lipid composition of photosynthetic systems, in:“Biochemistry of Chloroplasts, volume 1”, T.W. Goodwin, ed., pp. 195–200, Academic Press, London.Google Scholar
  2. Andrews, J., and Mudd, J.B., 1984, Phosphatidylglycerol synthesis in pea chloroplasts:characterization and localization, in: “Structure, Function and Metabolism of Plant Lipids”, P.A. Siegenthaler, ed., in press, Elsevier, Amsterdam.Google Scholar
  3. Bertrams,M., and Heinz, E., 1979, Soluble, isomeric forms of glycerophosphate acyltransferase in chloroplasts, in:“Advances in the Biochemistry and Physiology of Plant Lipids”(L.A. Appelqvist and C. Liljenberg, eds.), pp. 139–144,Elsevier/ North-Holland, Amsterdam.Google Scholar
  4. Billecocq, A., 1974, Structure des membranes biologiques:Localisation des galactosyldiglycérides dans les chloroplastes au moyen des anticorps spécifiques. II.Etude en microscopie électronique à l’aide d’un marquage à la peroxydase, Biochim. Biophys. Acta 352:245–251.PubMedCrossRefGoogle Scholar
  5. Billecocq, A., 1975, Structure des membranes biologiques:Localisation du sulfoquinovosyldiglycéride dans les diverses membranes des chloroplastes au moyen des anticorps spécifiques, Ann. Immunol. (Inst. Pasteur) 126c:337–352.Google Scholar
  6. Billecocq, A., Douce, R., and Faure, M., 1972, Structure des membranes biologiques:Localisation des galactosyldiglycérides dans les chloroplastes au moyen des anticorps spécifiques, C.R. Acad. Sci.,275:1135–1137.Google Scholar
  7. Bligny, R., and Douce, R., 1980, A precise localization of cardio- lipin in plant cells, Biochim. Biophys. Acta, 617:254–263.Google Scholar
  8. Block, M.A., Dorne, A.-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. 258:13273–13280.Google Scholar
  9. Block, M.A., Dorne, A.-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. 258:13281–13286.Google Scholar
  10. Block, M.A., Dorne, A.-J., and Douce, R., 1983c, The phosphatidic acid phosphatase of the chloroplast envelope is located on the inner envelope membrane, FEBS Lett., 169:111–115.CrossRefGoogle Scholar
  11. Block, M.A., Dorne, A.-J., and Douce, R., 1983d, The acyl-CoA synthetase and the acyl-CoA thioesterase are located respectively on the outer and on the inner membrane of the chloroplast envelope, FEBS Lett. 153:377–381.CrossRefGoogle Scholar
  12. Bogorad, L., 1975, Evolution of organelles and eukaryotic genomes, Science, 188:891–898.PubMedCrossRefGoogle Scholar
  13. Carde, J.P., Joyard, J., and Douce, R., 1982, Electron microscopic studies of envelope membranes from spinach plastids, Biol. Cell., 44:315–324.Google Scholar
  14. Chua, N.-H., and Gillham, N.W., 1977, The sites of synthesis of the principal thylakoid membrane polypeptides in Ch amydamanas Azinhandii, J. Cell Biol., 74:441–452.PubMedCrossRefGoogle Scholar
  15. Chua, N.-H., and Schmidt, G.W., 1979, Transport of proteins into chloroplasts and mitochondria, J. Cell Biol., 81:461–483.PubMedCrossRefGoogle Scholar
  16. Cline, K., Andrews, J., Mersey, B., Newcomb, E.H. and Keegstra, K., 1981, Separation and characterization of inner and outer envelope membranes of pea chloroplasts, Proc. Natl. Acad. Sci. U.S.A., 78:3595–3599.PubMedCrossRefGoogle Scholar
  17. DiRienzo, J.M., Nakamura, K., and Inouye, M., 1978, The outer membrane proteins of gram-negative bacteria:Biosynthesis, assembly, and functions, Ann. Rev. Biochem., 47:481–532.PubMedCrossRefGoogle Scholar
  18. Dorne, A.-J., Block, M.A., Joyard, J., and Douce, R., 1982a, Studies on the localization of enzymes involved in galactolipid metabolism in chloroplast envelope membranes, in:Biochemistry and Metabolism of Plant Lipids“(J.F.G.M. Wintermans and P.J.C. Kuiper, eds.), pp. 153–164, Elsevier, Amsterdam.Google Scholar
  19. Dorne, A.-J., Block, M.A., Joyard, J., and Douce, R., 1984, Localization of phosphatidylcholine in chloroplast envelope membranes from spinach, in:“Structure, Function and Metabolism of Plant Lipids”, P.A. Siegenthaler, ed., in press, Elsevier, Amsterdam.Google Scholar
  20. Dorne, A.-J., Carde, J.P., Joyard, J., Börner, T., and Douce, R., 1982b, Polar lipid composition of a plastid ribosome-deficient barley mutant, Plant Physiol., 65:1467–1470.Google Scholar
  21. Douce, R., 1974, Site of biosynthesis of galactolipids in spinach chloroplasts, Science, 183:852–853.PubMedCrossRefGoogle Scholar
  22. Douce, R., and Guillot-Salomon, T., 1970, Sur l’incorporation de la radioactivité du in-glycerol 3-phosphate-14C dans le monogalactosyldiglycéride des plastes isolés, FEBS Lett., 11:121–126.PubMedCrossRefGoogle Scholar
  23. Douce, R., and Joyard, J., 1979, Structure and function of the plastid envelope, Adv. Bot. Res., 7:1–116.CrossRefGoogle Scholar
  24. Douce, R., and Joyard, J., 1980, Plant galactolipids, in:The Biochemistry of Plants, Vol. 4, Lipids:Structure and Function“(P.K. Stumpf, ed.), pp. 321–362, Academic Press, New-York.Google Scholar
  25. Douce, R., and Joyard, J., 1981, Does the plastid envelope derive from the endoplasmic reticulum ?, Trends Biochem. Sci. 6:237–239.CrossRefGoogle Scholar
  26. Douce, R., and Joyard, J., 1982, Purification of the chloroplast envelope, in:’Methods in Chloroplast Molecular Biology“(M. Edelman, R. Hallick, and N.-H. Chua, eds.), pp. 239–256, Elsevier/NorthHolland, Amsterdam.Google Scholar
  27. Douce, R., Christensen, E.L., and Bonner, W.D., 1972, Preparation of intact plant mitochondria, Biochim. Biophys. Acta, 275:148–159.PubMedCrossRefGoogle Scholar
  28. Douce, R., Holtz, R.B., and Benson, A.A., 1973, Isolation and properties of the envelope of spinach chloroplasts, J. Biol. Chem., 248:7215–7222.PubMedGoogle Scholar
  29. Douce, R., Block, M.A., Dorne, A.J., and Joyard, J., 1984, The plastid envelope membranes:Their structure, composition, and role in chloroplast biogenesis, in:“Subcellular Biochemistry, Volume 10”, D.B. Roodyn, ed., pp. 1–84, Plenum, New-York.Google Scholar
  30. Dubacq, J.-P., Drapier, D., and Trémolières, A., 1983, Polyunsaturated fatty acid synthesis by a mixture of chloroplasts and microsomes from spinach leaves:Evidence for two distinct pathways of the synthesis of trienoic acids, Plant Cell Physiol. 24:1–9.Google Scholar
  31. Edelman, M., 1981, Nucleic acids of chloroplasts and mitochondria, in:The Biochemistry of Plants, Vol. 6, Proteins and Nucleic Acids“(A. Marcus, ed.), pp.249–301, Academic Press, New-York.Google Scholar
  32. Ellis, R.J., 1976, Protein and nucleic acid synthesis by chloroplasts, in:The Intact Chloroplast“(J. Barber, ed.), pp. 335–364, Elsevier, Amsterdam.Google Scholar
  33. Ellis, R.J., 1981, Chloroplast proteins:Synthesis, transport, and assembly, Annu. Rev. Plant Physiol., 32:111–137.CrossRefGoogle Scholar
  34. Flügge, U.I., 1982, Biogenesis of the chloroplast phosphate trans-locator, FEBS Lett., 140:273–276.CrossRefGoogle Scholar
  35. Flügge, U.I., and Benz, R., 1984, Pore-forming activity in the outer membrane of the chloroplast envelope, FEBS Lett., 69:85–89.CrossRefGoogle Scholar
  36. Flügge, U.I., and Heldt, H.W., 1976, Identification of a protein involved in phosphate transport of chloroplasts, FEBS Lett., 68:259–262PubMedCrossRefGoogle Scholar
  37. Fredrick, J.F., 1981, Origins and evolution of eukaryotic intracellular organelles, Ann. N.Y. Acad. Sci.,361.Google Scholar
  38. Frentzen, M., Heinz, E., McKeon, T., and Stumpf, P.K., 1982, De novo-biosynthesis of galactolipid molecular species by reconstituted enzyme systems from chloroplasts, in:Biochemistry and Metabolism of Plant Lipids“(J.F.G.M. Wintermans and P.J.C. Kuiper, eds.), pp. 141–152, Elsevier, AmsterdamGoogle Scholar
  39. Gardiner, S.E., and Roughan, P.G., 1983, Relationship between fattyacyl composition of diacylgalactosylglycerol and turnover of chloroplast phosphatidate, Biochem. J., 210:949–952.PubMedGoogle Scholar
  40. Haas, R., Siebertz, H.P., Wrage, K., and Heinz, E., 1980, Localization of sulfolipid labelling within cells and chloroplasts, Planta, 148:238–244.CrossRefGoogle Scholar
  41. Hartmann-Bouillon, M.-A., 1980, Les stérols des membranes des plantes:Distribution et métabolisme, Thèse de Doctorat d’Etat, Université de Strasbourg, France.Google Scholar
  42. Harwood, J.L., 1979, The synthesis of acyl lipids in plant tissues, Prog. Lipid Res., 18:55–86.PubMedCrossRefGoogle Scholar
  43. Heber, U., and Heldt, H.W., 1981, The chloroplast envelope:Structure, function and role in leaf metabolism, Annu. Rev. Plant Physiol., 32:139–168.CrossRefGoogle Scholar
  44. Heber, U., and Walker, D.A., 1979, The chloroplast envelope-Barrier or bridge?, Trends Biochem. Sci., 4:393–421.CrossRefGoogle Scholar
  45. Heinz, E., 1977, Enzymatic reactions in galactolipid biosynthesis, in:Lipids and Lipid Polymers in Higher Plants“(M. Tevini and H.K. Lichtenthaler, eds.), pp. 102–120, Springer-Verlag, Berlin.CrossRefGoogle Scholar
  46. Heinz, E., and Roughan, P.G., 1982, De novo synthesis, desaturation and acquisition of monogalactosyldiacylglycerol by chloroplasts from “16:3”- and “18:3” -plants, in:Biochemistry and Metabolism of Plant Lipids“(J.F.G.M. Wintermans and P.J.C. Kuiper, eds.), pp. 169–182, Elsevier, Amsterdam.Google Scholar
  47. Hermann, R.G., Seyer, P., Schedel, R., Gordon, K., Bisanz, C., Winter, P., Hildebrandt, J.W., Wlaschek, M., Alt,J., Driesel, A.J., and Sears, B.B., 1980, The plastid chromosomes of several dicotyledons, in:Biological Chemistry of Organelle Forma- tion“(T. Bücher, W. Sebald, and H. Weiss, eds.), pp. 97–112, Springer-Verlag, Berlin.Google Scholar
  48. Hoober, J.K., 1976, Protein synthesis in chloroplasts, in:Protein Synthesis, Vol. 2“(E.H. McConkey, ed.), pp. 169–248, Marcel Dekker, New-York and Basel.Google Scholar
  49. Hurkmann, W.J., Morré, D.J., Bracker, C.E., and Mollenhauer, H.H., 1979, Identification of etioplast membranes in fraction from soybean hypocotyls, Plant Physiol., 257:1095–1101.Google Scholar
  50. Joyard, J., 1979, L’enveloppe des chloroplastes, Thèse de Doctorat d’Etat, Université de Grenoble, France.Google Scholar
  51. Joyard, J., and Douce, R., 1976, L’enveloppe des chloroplastes est-elle capable de synthétiser la phosphatidylcholine?, C.R. Acad. Sci. 282:1515–1518.Google Scholar
  52. Joyard, J., and Douce, R., 1977, Site of synthesis of phosphatidic acid and diacylglycerol in spinach chloroplasts, Biochim. Biophys. Acta 486:273–285.PubMedGoogle Scholar
  53. Joyard, J., and Douce, R., 1979, Characterization of a phosphatidate phosphatase activity associated with chloroplast envelope membranes, FEBS Lett., 102:147–150.PubMedCrossRefGoogle Scholar
  54. Joyard, J., Chuzel, M., and Douce, R., 1979, Is the chloroplast envelope a site of galactolipid synthesis? Yes!, inAdvances in the Biochemistry and Physiology of Plant Lipids“(L.A. Appelqvist and C. Liljenberg, eds.), pp. 181–186, Elsevier/North-Holland, Amsterdam.Google Scholar
  55. Joyard, J., Grossman, A.R., Bartlett, S.G., Douce, R., and Chua, N.H., 1982, Characterization of envelope membrane polypeptides from spinach chloroplasts, J. Biol. Chem., 257:1095–1101.PubMedGoogle Scholar
  56. Joyard, J., Billecocq, A., Bartlett, S.G., Block, M.A., Chua, N.H., and Douce, R., 1983, Localization of polypeptides to the cytosolic side of the outer envelope membrane of spinach chloroplasts, J. Biol. Chem., 258:10000–10006.PubMedGoogle Scholar
  57. Keegstra, K., Werner-Washburne, M., Cline, K., and Andrews, J., 1984, The chloroplast envelope:is it homologous with the double membranes of mitochondria and gram-negative bacteria ? J. Cell. Biochem., 24:55–68.PubMedCrossRefGoogle Scholar
  58. Lewin, R.A., 1981, Prochloron and the theory of symbiogenesis, in: “Origins and evolution of eukaryotic intracellular organelles”, J.F. Fredrick, ed., pp. 325–329, Ann. N.Y. Acad. Sci., New-York.Google Scholar
  59. Mereschkowsky, C., 1905, Ober natur and ursprung der chromatophoren im Pflanzenreiche, Biol. Zentralbl., 25:593–604.Google Scholar
  60. Moeller, C.H., and Mudd, J.B., 1982, Localization of filipin-sterol complexes in the membranes of Beta vu,2gatcds roots and Sp,&w a. otenacea chloroplasts, Plant Physiol., 70:1554–1561.PubMedCrossRefGoogle Scholar
  61. Mudd, J.B., and de Zacks, R., 1981, Synthesis of phosphatidylglycerol by chloroplasts from leaves of Sp-,nace,a otehacea L. (spinach), Arch. Biochem. Biophys., 209:584–591.PubMedCrossRefGoogle Scholar
  62. Mudd, J.B., 1982, Lipid Metabolism, in:“On the origins of chloro- plasts”, J.A. Schiff, ed., pp. 131–148, Plenum, New-York.Google Scholar
  63. Murata, N., and Sato, N., 1982, In vivo synthesis of lipids in the blue-green alga, Anabaena vatiabitbs, in:“Biochemistry and Metabolism of Plant Lipids”(J.F.G.M. Wintermans and P.J.C. Kuiper, eds.), pp. 165–168, Elsevier, Amsterdam.Google Scholar
  64. Murata, N., Sato, N., Ornata, T., and Kuwabara, T., 1981, Separation and characterization of thylakoid and cell envelope of the blue green alga (cyanobacterium) Anacyb s nidatan6. Plant Cell Physiol., 22:855–866.Google Scholar
  65. Nichols, B.W., Harris, R.V., and James, A.T., 1965, The lipid metabolism of blue-green algae, Biochem. Biophys. Res. Commun., 20:256–262.PubMedCrossRefGoogle Scholar
  66. Ohlrogge, J.B., 1982, Fatty acid synthetase:Plant and bacteria have similar organization. Trends Biochem. Sci., 7:386–387.CrossRefGoogle Scholar
  67. Ornata, T., and Murata, N., 1983, Isolation and characterization of the cytoplasmic membranes from the blue-green alga (cyanobacterium) Anacy4tbs nidutan4, Plant Cell Physiol., 24:1101–1112.Google Scholar
  68. Ongun, A., and Mudd, J.B., 1968, Biosynthesis of galactolipids in plants, J. Biol. Chem. 243:263–275.Google Scholar
  69. Peschek, G.A., 1984, Structure and function of respiratory membranes in cyanobacteria (blue-green algae), in: “Subcellular Biochemistry, Volume 10”, D.B. Roodyn, ed., pp. 85–191, Plenum, New-York.CrossRefGoogle Scholar
  70. Roughan, P.G., and Slack, C.R., 1982, Cellular organization of glycerolipid metabolism, Annu. Rev. Plant Physiol., 33:97–132.CrossRefGoogle Scholar
  71. Sato, N., and Murata, N., 1982a, Lipid biosynthesis in the blue- green alga, Anabaena vcvriabiLL4. I. Lipid classes, Biochim. Biophys. Acta, 710:271–278.Google Scholar
  72. Sato, N., and Murata, N., 1982b, Lipid biosynthesis in the blue-green alga, Anabaena vc t iabi Ls. II. Fatty acids and molecular species, Biochim. Biophys. Acta, 710:279–289.Google Scholar
  73. Sato, N., and Murata, N., 1982c, Lipid biosynthesis in the blue-green alga, Anabaena vcv~ í ab í P,íß III. UDP-glucose:diacylglycerol glucosyltransferase in vitro. Plant Cell Physiol.,23:115–1120.Google Scholar
  74. Schimper, A.F.W., 1885, Untersuchungen über die chlorophyllkörner und die ihnen homologen gebilde, Jahrb. Wiss. Botan., 16:1–247.Google Scholar
  75. Schiff, J.A., 1982,“On the origins of chloroplasts, Elsevier/NorthHolland, New-York.Google Scholar
  76. Siebertz, H.P., Heinz, E., Linscheid, M., Joyard, J., and Douce, R., 1979, Characterization of lipids from chloroplast envelopes, Eur. J. Biochem., 101:429–438.PubMedCrossRefGoogle Scholar
  77. Soll, J., Schultz, G., Joyard, J., Douce, R., and Block, M.A., 1984, Localization and synthesis of prenylquinones in isolated outer and inner envelope membranes from spinach chloroplasts, in: “Structure, Function and Metabolism of Plant Lipids”, P.A. Siegenthaler, ed., in press. Elsevier, Amsterdam.Google Scholar
  78. Sparace, S.A., and Mudd, J.B., 1982, Phosphatidylglycerol synthesis in spinach chloroplasts:Characterization of the newly synthesized molecule, Plant Physiol., 70:1260–1264.PubMedCrossRefGoogle Scholar
  79. Stanier, R.Y., and Cohen-Bazire, G., 1977, Phototrophic prokaryotes-The cyanobacteria, Annu. Rev. Microbiol., 31:225–274.CrossRefGoogle Scholar
  80. Stumpf, P.K., 1980, Biosynthesis of saturated and unsaturated fatty acids, in: “The Biochemistry of Plants, Vol. 4, Lipids:Structure and Function” (P.K. Stumpf, ed.), pp. 177–204, Academic Press, New-York.Google Scholar
  81. Stumpf, P.K., Shimakata, T., Eastwell, K., Murphy, D.J., Liedvogel, B., Ohlrogge, J.B., and Kuhn, D.N., 1982, Biosynthesis of fatty acids in a leaf cell, in: “Biochemistry and Metabolism of Plant Lipids” (J.F.G.M. Wintermans and P.J.C. Kuiper, eds.), pp. 3–11, Elsevier, Amsterdam.Google Scholar
  82. Van Besouw, A., and Wintermans, J.F.G.M., 1978, Galactolipid formation in chloroplast envelopes. I. Evidence for two mechanisms in galactosylation, Biochim. Biophys. Acta, 529:44–53.PubMedGoogle Scholar
  83. Whatley, J.M., 1983, Plastids. Past, present and future, Int. Rev. Cyt., 514:329–373.Google Scholar
  84. Williams, J.P., Khan, M., and Mitchell, K., 1982, Galactolipid biosynthesis in Bnco5ica napwo and Utica /Çaba:A comparison of lipid biosynthesis in 16:3- and 18:3-plants, in: “Biochemistry and Metabolism of Plant Lipids” (J.F.G.M. Wintermans and P.J.C. Kuiper, eds.), pp:183–186, Elsevier, Amsterdam.Google Scholar
  85. Wirtz, K.W.A., 1974, Transfer of phospholipids between membranes, Biochim. Biophys. Acta, 344:95–117.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1985

Authors and Affiliations

  • Roland Douce
    • 1
  • Jacques Joyard
    • 1
  • Albert-Jean Dorne
    • 1
  • Maryse A. Block
    • 1
  1. 1.Physiologie Cellulaire Végétale (UA CNRS n° 576)DRF/BV, CENG and USMG, 85 XGrenoble cedexFrance

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