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.
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Abbreviations
- ER:
-
endoplasmic reticulum
References
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 1975
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)
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)
Frederick, S.E., Gruber, P.J., Newcomb, E.H.: Plant microbodies. Protoplasma 84, 1–29 (1975)
Frey-Wyssling, A., Grieshaber, E., Mühlethaler, K.: Origin of spherosomes in plant cells. J. Ultrastructure Res. 8, 506–516 (1963)
Frey-Wyssling, A., Mühlethaler, K.: Ultrastructural plant cytology. Amsterdam: Elsevier 1965
Gerhardt, B.: Microbodies/Peroxisomen pflanzlicher Zellen. Cell Biology Monographs, Vol. 5. Wien New York: Springer 1978
Gunning, B.E.S., Steer, M.W.: Plant Cell Biology, an Ultrastructural Approach. London: Arnold 1975
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 1975
Hock, B., Kühnert, E., Mohr, H.: Die Regulation von Fettabbau und Atmung bei Senfkeimlingen durch Licht (Sinapis alba L.) Planta 65, 129–138 (1965)
Jacks, T.J., Yatsu, L.Y., Altschul, A.M.: Isolation and characterization of peanut spherosomes. Plant Physiol. 42, 585–597 (1967)
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)
Kleinig, H., Steinki, C., Kopp, C., Zaar, K.: Oleosomes (spherosomes) from Daucus carota suspension culture cells. Planta 140, 233–237 (1978)
Matile, P.: The lytic compartment of plant cells. Cell Biology Monographs, Vol. 1. Wien New York: Springer 1975
Mohr, H.: Untersuchungen zur phytochrominduzierten Photomor-phogenese des Senfkeimlings (Sinapis alba L.). Z. Pflanzenphysiol. 54, 63–83 (1966)
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)
Moreau, R.A., Huang, A.H.C.: Gluconeogenesis from storage wax in the cotyledons of jojoba seedlings. Plant Physiol. 60, 329–333 (1977)
Muto, S., Beevers, H.: Lipase activities in castor bean endosperm during germination. Plant Physiol. 54, 23–28 (1974)
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)
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)
Perner, E.S.: Die Sphärosomen (Mikrosomen) pflanzlicher Zellen. Protoplasma 42, 457–481 (1953)
Ray, P.: Auxin-binding sites of maize coleoptiles are localized on membranes of the endoplasmic reticulum. Plant Physiol. 59, 594–599 (1977)
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)
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)
Rickson, F.R.: The ultrastructure of Acacia cornigera L. Beltian body tissue. Amer J. Bot. 62, 913–922 (1975)
Schwarzenbach, A.M.: Observations on spherosomal membranes. Cytobiol. 4, 145–147 (1971)
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)
Schopfer, P., Bajracharya, D., Falk, H., Thien, W.: Phytochromgesteuerte Entwicklung von Zellorganellen (Plastiden, Microbodies, Mitochondrien). Ber. deutsch. Bot. Ges. 88, 245–268 (1975)
Smith, C.G.: The ultrastructural development of spherosomes and oil bodies in the developing embryo of Crambe abyssinica. Planta 119, 125–142 (1974)
Sorokin, H.P.: The spherosomes and the reserve fat in plant cells. Amer. J. Bot. 54, 1008–1016 (1967)
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 1977
Theimer, R.R., Rosnitschek, I.: Development and intracellular localization of lipase activity in rape seed (Brassica napus L.) cotyledons. Planta 139, 249–256. (1978)
Wanner, G., Theimer, R.R.: Membranous appendices of spherosomes (oleosomes). Possible role in fat utilization in germinating oil seeds. Planta 40, 163–169 (1978)
Yatsu, L.Y., Jacks, T. J.: Spherosome membranes. Half unit-membranes. Plant Physiol. 49, 937–943 (1972)
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)
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Bergfeld, R., Hong, YN., Kühnl, T. et al. Formation of oleosomes (storage lipid bodies) during embryogenesis and their breakdown during seedling development in cotyledons of Sinapis alba L.. Planta 143, 297–307 (1978). https://doi.org/10.1007/BF00392002
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DOI: https://doi.org/10.1007/BF00392002