Advertisement

Planta

, Volume 143, Issue 3, pp 297–307 | Cite as

Formation of oleosomes (storage lipid bodies) during embryogenesis and their breakdown during seedling development in cotyledons of Sinapis alba L.

  • R. Bergfeld
  • Y.-N. Hong
  • T. Kühnl
  • P. Schopfer
Article

Abstract

Electron microscopic and biochemical investigations of developing embryonic mustard cotyledons provided no evidence for the widely accepted hypothesis that oleosomes of fat-storing tissues originate from the endoplasmic reticulum and are surrounded by a unit- or half-unit membrane. In contrast, it was found that the first lipid droplets appear (about 12–14 d after pollination) in the ground cytoplasm near the surface of plastids. Subsequently these nascent lipid droplets, which lack any detectable boundary structure at this stage, become encircled by a cisterna of rough endoplasmic reticulum. At the same time an osmiophilic coat of about 3 nm thickness becomes detectable at the lipid/water interface. In the cotyledon cells of germinating seedlings a centrifugally moving front of fat degradation moves from the central vacuoles(s) towards the cell periphery, leaving behind collapsed coats of oleosomes which are depleted of their lipid contents (saccules). Although saccules appear tripartite in cross section, they are structurally different from endoplasmic reticulum membranes. The oleosome coats can be isolated from oleosome preparations by extracting lipids with organic solvents. The coat material is insoluble in detergents like Triton X-100 or deoxycholate and shows a tripartite, lamellar structure (similar to collapsed saccules) under the electron microscope. Upon dissolution with dodecylsulfate, polyacrylamide gel electrophoresis revealed a polypeptide composition (9 major bands) which is qualitatively different from that of the endoplasmic reticulum membrane. Also the buoyant densities of defatted oleosome coats and defatted endoplasmic reticulum membranes are very different. It is concluded that oleosome lipids accumulate in the ground cytoplasm and are bounded by a lamellar structure originating de novo from proteinaceous elements synthesized by specific regions of the endoplasmic reticulum.

Key words

Embryogenesis Lipid bodies Oleosomes Sinapis Spherosomes 

Abbreviation

ER

endoplasmic reticulum

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Appelqvist, L.-Å.: Biochemical and structural aspects of storage and membrane lipids in developing oil seeds. In: Rec. Adv. Chem. Biochem. Plant Lipids. Galliard, T., Mercer, E.I., eds. pp. 247–286. London New York San Francisco, Academic Press 1975Google Scholar
  2. Bowden, L., Lord, J.M.: Similarities in the polypeptide composition of glyoxysomal and endoplasmic-reticulum membranes from castor-bean endospern. Biochem. J. 154, 491–499 (1976)Google Scholar
  3. Fairbanks, G., Steck, T.L., Wallach, D.F.H.: Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry 10, 2606–2617 (1971)Google Scholar
  4. Frederick, S.E., Gruber, P.J., Newcomb, E.H.: Plant microbodies. Protoplasma 84, 1–29 (1975)Google Scholar
  5. Frey-Wyssling, A., Grieshaber, E., Mühlethaler, K.: Origin of spherosomes in plant cells. J. Ultrastructure Res. 8, 506–516 (1963)Google Scholar
  6. Frey-Wyssling, A., Mühlethaler, K.: Ultrastructural plant cytology. Amsterdam: Elsevier 1965Google Scholar
  7. Gerhardt, B.: Microbodies/Peroxisomen pflanzlicher Zellen. Cell Biology Monographs, Vol. 5. Wien New York: Springer 1978Google Scholar
  8. Gunning, B.E.S., Steer, M.W.: Plant Cell Biology, an Ultrastructural Approach. London: Arnold 1975Google Scholar
  9. Harwood, J.L.: Fatty acid biosynthesis. In: Rec. Adv. Chem. Biochem. Plant Lipids. Galliard, T., Mercer, E.I., eds. pp. 43–93. London New York San Francisco, Academic Press 1975Google Scholar
  10. Hock, B., Kühnert, E., Mohr, H.: Die Regulation von Fettabbau und Atmung bei Senfkeimlingen durch Licht (Sinapis alba L.) Planta 65, 129–138 (1965)Google Scholar
  11. Jacks, T.J., Yatsu, L.Y., Altschul, A.M.: Isolation and characterization of peanut spherosomes. Plant Physiol. 42, 585–597 (1967)Google Scholar
  12. Kleinig, H., Liedvogel, B.: Fatty acid synthesis by isolated chromoplasts from the daffodil, [14C] acetate incorporation and distribution of labelled acids. Eur. J. Biochem. 83, 499–505 (1978)Google Scholar
  13. Kleinig, H., Steinki, C., Kopp, C., Zaar, K.: Oleosomes (spherosomes) from Daucus carota suspension culture cells. Planta 140, 233–237 (1978)Google Scholar
  14. Matile, P.: The lytic compartment of plant cells. Cell Biology Monographs, Vol. 1. Wien New York: Springer 1975Google Scholar
  15. Mohr, H.: Untersuchungen zur phytochrominduzierten Photomor-phogenese des Senfkeimlings (Sinapis alba L.). Z. Pflanzenphysiol. 54, 63–83 (1966)Google Scholar
  16. Mollenhauer, H.H., Totten, C.: Studies on seeds. II. Origin and degradation of lipid vesicles in pea and bean cotyledons. J. Cell Biol. 48, 395–405 (1971)Google Scholar
  17. Moreau, R.A., Huang, A.H.C.: Gluconeogenesis from storage wax in the cotyledons of jojoba seedlings. Plant Physiol. 60, 329–333 (1977)Google Scholar
  18. Muto, S., Beevers, H.: Lipase activities in castor bean endosperm during germination. Plant Physiol. 54, 23–28 (1974)Google Scholar
  19. Neville, D.M.: Molecular weight determination of protein-dodecylsulfate complexes by gel electrophoresis in a discontinuous buffer system. J. Biol. Chem. 246, 6328–6334 (1971)Google Scholar
  20. Ory, R.L., Yatsu, L.W., Kircher, H.W.: Association of lipase activity with the spherosomes of Ricinus communis. Arch. Biophys. Biochem. 123, 255–264 (1968)Google Scholar
  21. Perner, E.S.: Die Sphärosomen (Mikrosomen) pflanzlicher Zellen. Protoplasma 42, 457–481 (1953)Google Scholar
  22. Ray, P.: Auxin-binding sites of maize coleoptiles are localized on membranes of the endoplasmic reticulum. Plant Physiol. 59, 594–599 (1977)Google Scholar
  23. Rest, J.A., Vaughan, J.G.: The development of protein and oil bodies in the seed of Sinapis alba L. Planta 105, 245–262 (1972)Google Scholar
  24. Reynolds, E.S.: The use of lead citrate at high pH as an electronopaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963)Google Scholar
  25. Rickson, F.R.: The ultrastructure of Acacia cornigera L. Beltian body tissue. Amer J. Bot. 62, 913–922 (1975)Google Scholar
  26. Schwarzenbach, A.M.: Observations on spherosomal membranes. Cytobiol. 4, 145–147 (1971)Google Scholar
  27. Schopfer, P., Bajracharya, D., Bergfeld, R., Falk, H.: Phytochrome-mediated transformation of glyoxysomes into peroxisomes in the cotyledons of mustard (Sinapis alba L.) seedlings. Planta 133, 73–80 (1976)Google Scholar
  28. Schopfer, P., Bajracharya, D., Falk, H., Thien, W.: Phytochromgesteuerte Entwicklung von Zellorganellen (Plastiden, Microbodies, Mitochondrien). Ber. deutsch. Bot. Ges. 88, 245–268 (1975)Google Scholar
  29. Smith, C.G.: The ultrastructural development of spherosomes and oil bodies in the developing embryo of Crambe abyssinica. Planta 119, 125–142 (1974)Google Scholar
  30. Sorokin, H.P.: The spherosomes and the reserve fat in plant cells. Amer. J. Bot. 54, 1008–1016 (1967)Google Scholar
  31. Stumpf, P.K.: Lipid biosythesis in developing seeds. In: Lipids and Lipid Polymers in Higher Plants, Tevini, M., Lichtenthaler, H.K., eds. pp. 75–84. Berlin Heidelberg New York: Springer 1977Google Scholar
  32. Theimer, R.R., Rosnitschek, I.: Development and intracellular localization of lipase activity in rape seed (Brassica napus L.) cotyledons. Planta 139, 249–256. (1978)Google Scholar
  33. Wanner, G., Theimer, R.R.: Membranous appendices of spherosomes (oleosomes). Possible role in fat utilization in germinating oil seeds. Planta 40, 163–169 (1978)Google Scholar
  34. Yatsu, L.Y., Jacks, T. J.: Spherosome membranes. Half unit-membranes. Plant Physiol. 49, 937–943 (1972)Google Scholar
  35. Yatsu, L.Y., Jacks, T.J., Hensarling, T.P.: Isolation of spherosomes (oleosomes) from onion, cabbage, and cottonseed tissue. Plant Physiol. 48, 675–682 (1971)Google Scholar

Copyright information

© Springer-Verlag 1978

Authors and Affiliations

  • R. Bergfeld
    • 1
  • Y.-N. Hong
    • 1
  • T. Kühnl
    • 1
  • P. Schopfer
    • 1
  1. 1.Biologisches Institut IIUniversität FreiburgFreiburgFederal Republic of Germany

Personalised recommendations