Abstract
Maturing embryos of 16 oil plants, anise suspension culture cells, and Neurospora crassa cells were prepared for electron microscopy at different stages during massive lipid accumulation. Lipid-rich structures of certain species were best preserved by dehydration of fixed tissues in ethanol without propylene oxide, embedding in Spurr's Medium, and polymerization at room temperature. In all cells examined, spherical lipid bodies (spherosomes) showed a moderately osmiophilic, amorphous matrix and displayed a delimiting half-unit membrane when sectioned medially. Associations with the endoplasmic reticulum (ER) were viewed at any stage during lipid body development but with different frequency in the different plant species. Plastids of fat-storing cells exhibited conspicuously undulate outer and inner envelope membranes that formed multiple contact sites with each other and protuberances into both cytoplasm and stroma. Some species, e.g., Linum, have plastids with tubular structures that connect the inner membrane to the thylakoid system; in addition, in the stroma vesicles fusing with or apparently passing through the envelope were observed. The outer envelope membrane may be associated with ER-like cytoplasmic membrane structures. In addition, lipid bodies of various sizes were found in contact with the plastid envelope. The ultrastructural observations are interpreted to match the published biochemical evidence, indicating that both plastids and ER may be involved in the synthesis of storage lipids and lipid body production.
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Bergfeld, R., Hong, Y.-N., Kühnl, T., Schopfer, P. (1978) Formation of oleosomes (storage lipid bodies) during embryogenesis and their breakdown during seedling development in cotyledons of Sinapis alba L. Planta 143, 297–307
Cohen, W.S., Nathanson, B., White, J.E., Brody, M. (1969) Fatty acids as model systems for the action of Ricinus leaf extract on higher plant chloroplasts and algae. Arch. Biochem. Biophys. 135, 21–27
Falk, H. (1976) Chromoplasts of Tropaeolum majus L. Structure and development. Planta 128, 15–22
Frey-Wyssling, A., Grieshaber, E., Mühlethaler, K. (1963) Origin of spherosomes in plant cells. J. Ultrastruct Res. 8, 506–516
Galliard, T., Stumpf, P.K. (1966) Fat metabolism in higher plants XXX. Enzymatic synthesis of ricinoleic acid by a microsomal preparation from developing Ricinus communis seeds. J. Biol. Chem. 241, 5806–5812
Huber, J., Constabel, F., Gamborg, O.L. (1978) A cell counting procedure applied to embryogenesis in cell suspension culture of anise (Pimpinella anisum L.) Plant Sci. Lett. 12, 209–215
Kanangara, C.G., Stumpf, P.K. (1972) Fat metabolism in higher plants L. The biosynthesis of polyunsaturated fatty acids by isolated spinach chloroplasts. Arch. Biochem. Biophys. 148, 414–424
Kleinig, H., Liedvogel, B. (1978) Fatty acid synthesis by isolated chromoplasts from the daffodil. [14C] acetate incorporation and distribution of labelled acids. Eur J. Biochem. 83 499–505
Mollenhauer, H.H., Totten, C. (1971) Studies on seeds. II. Origin and degradation of lipid vesicles in pea and bean cotyledons. J. Cell Biol. 48, 395–405
Morgan, T.E., Huber, G.L. (1967) Loss of lipid during fixation for electron microscopy. J. Cell Biol. 32, 757–760
Morré, D.J., Mollenhauer, H.H. (1974) The endomembran concept: a functional integration of endoplasmic reticulum and Golgi apparatus. In: Dynamic aspects of plant ultrastructure, pp. 84–137, Robards, A.W., ed. McGraw-Hill, London
Nothelfer, H.G., Barckhaus, R.H., Spener, F. (1977) Localization and characterization of the farty acid synthesizing system in cells of Glycine max (soybean) suspension cultures. Biochim. Biophys. Acta 489, 370–380
Ohlrogge, J.B., Kuhn, D.N., Stumpf, P.K. (1979) Subcellular localization of acyl carrier protein in leaf protoplasts of Spinacia oleracea. Proc. Natl. Acad. Sci. USA 76, 1194–1198
Panter, R.A., Boardman, N.K. (1973) Lipid biosynthesis by isolated plastids from greening pea, Pisum sativum. J. Lipid Res. 14, 664–671
Porra, R.J. (1979) Formation of phospholipids from sn-glycerol-3-phosphate and free fatty acids or their derivatives by homogenates of soybean cotyledons. Phytochemisty 18, 1651–1656
Rest, J.A., Vaughan, J.G. (1972) The development of protein and oil bodies in the seed of Sinapis alba L. Planta 105, 245–262
Roughan, P.G., Slack, C.R. (1977) Long-Chain acyl-coenzyme A synthetase activity of spinach chloroplasts is concentrated in the envelope. Biochem. J. 162, 457–459
Schwarzenbach, A.M. (1971) Observations on spherosomal membranes. Cytobiologie 4, 145–147
Shine, W.E., Mancha, M., Stumpf, P.K. (1976) Fat metabolism in higher plants. Differential incorporation of acyl-coenzyme A and acyl-acyl carrier proteins into plant microsomal lipids. Arch. Biochem. Biophys. 173, 472–479
Sitte, P. (1977) Functional organization of biomembranes. In: Lipids and lipid polymers in higher plants, pp. 1–28, Tevini, M., Lichtenthaler, H.K., eds. Springer, Berlin Heidelberg New York
Slack, C.R., Roughan, P.G., Terpstra, J. (1976) Some properties of a microsomal oleate desaturase from leaves. Biochem. J. 155, 71–80
Smith, C.G. (1974) The ultrastructural development of spherosomes and oil bodies in the developing embryo of Crambe abyssinica Planta 119, 125–142
Spurr, A.R. (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31–43
Stein, O., Stein, Y. (1967a) Lipid synthesis, intracellular transport, storage and secretion. I. Electron microscopic radio autographic study of liver after injection of tritiated palmitate or glycerol in fasted and ethanol-treated rats. J. Cell. Biol. 33, 319–339
Stein, O., Stein, Y. (1967b) Lipid synthesis, intracellular transport and secretion. II. Electron microscopic radioautographic study of the mouse lactating mammary gland. J. Cell Biol. 34, 251–263
Stumpf, P.K. (1976) Lipid metabolism. In: Plant biochemistry, pp. 427–461, Bonner, J., Varner, J.E., eds. Academic Press, New York London
Stumpf, P.K. (1977) Lipid biosynthesis in developing seeds. In: Lipids and lipid polymers in higher plants, pp. 75–84, Tevini, M., Lichtenthaler, H.K., eds. Springer, Berlin Heidelberg New York
Stumpf, P.K., Boardman, N.K. (1970) Fat metabolism in higher plants XXXIX. Effect of adenosine triphosphate and Triton X-100 on lipid synthesis by isolated spinach chloroplasts. J. Biol. Chem. 245, 2579–2587
Stumpf, P.K., James, A.T. (1963) The biosynthesis of long-chain fatty acids by lettuce chloroplast preparations. Biochim. Biophys. Acta 70, 20–32
Stymne, S., Appelqvist, L.-A. (1978) The biosynthesis of linoleate from oleoyl-CoA via oleoyl-phosphatidylcholine in microsomes of developing saffower seeds. Eur. J. Biochem. 90, 223–229
Swanson, E.S., Thomson, W.W., Mudd, J.B. (1973) The effect of lipid extraction on electron-microscopic images of plant membranes. Can. J. Bot. 51, 1221–1229
Theimer, R.R., Anding, G., Matzner, P. (1976) Kinetin action on the development of microbody enzymes in sunflower cotyledons in the dark. Planta 128, 41–47
Theimer, R.R., Wanner, G., Anding, G. (1978) Isolation and biochemical properties of two types of microbody from Neurospora crassa cells. Cytobiologie 18, 132–144
Tremolieres, A., Mazliak, P. (1974) Biosynthetic pathway of α-linolenic acid in developing pea leaves. In vivo and in vitro study. Plant. Sci. Lett. 2, 193–201
Wanner, G., Theimer, R.R. (1978) Membranous appendices of spherosomes (oleosomes). Possible role in fat utilization in germinating oil seeds. Planta 140, 163–169
Weaire, P.J., Kekwick, R.G.O. (1975) The synthesis of fatty acids in avocado mesocarp and cauliflower bud tissue. Biochem. J. 146, 425–437
Yamada, M., Usami, Q. (1975) Long chain fatty acid synthesis in developing castor bean seeds. IV. The synthetic system in proplastids. Plant Cell Physiol. 16, 879–884
Yatsu, L.Y., Jacks, T.J. (1972) Spherosome membranes. Plant Physiol. 49, 937–947
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Wanner, G., Formanek, H. & Theimer, R.R. The ontogeny of lipid bodies (spherosomes) in plant cells. Planta 151, 109–123 (1981). https://doi.org/10.1007/BF00387812
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DOI: https://doi.org/10.1007/BF00387812