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Studies of Budding and Cell Wall Structure of Yeast

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Studies of Budding and Cell Wall Structure of Yeast STUDIES OF BUDDING AND CELL WALL STRUCTURE OF YEAST ELECTRON MICROSCOPY OF THIN SECTIONS' HILDA D. AGAR AND H. C. DOUGLAS Department of Microbiology, University of Washington School of Medicine, Seattle, Washington Received for publication April 15, 1955 Observations of intact yeast cells with the fixation times resulted in swelling, vacuolization, electron microscope have yielded little informa- and disruption of the cells. tion on cellular structure because of the im- Following fixation, the cells were dehydrated penetrability of the cells to the electron beam. by passage through a graded series of ethanol The development of techniques for the prepara- concentrations, impregnated with methacrylate tion of ultra-thin sections promises to obviate monomer, and polymerized in gelatin capsules this difficulty, and several papers have already as described by Newman et al. (1949). A mixture appeared in which this approach has been ap- of 4 parts N-butyl methacrylate and 1 part plied in studies of the structure of microorganisms methyl methacrylate monomer gave blocks of (Chapman and Hillier, 1953; Birch-Anderson the most satisfactory hardness for thin sectioning. et al., 1953; Wolken and Palade, 1953; Gustafson Sections were cut with a modified Spencer et al., 1954). Rotary Microtome (advanced by thermal ex- In this paper we describe details of the budding pansion) and more recently with a Porter Blum process and the structure of the cell wall of microtome.2 Glass knives prepared as described Saccharomyces cerevisiae as observed in thin by Latta and Hartmann (1950) were used with sections of intact cells and purified cell walls. both microtomes. The sections, as cut, were floated off on the surface of a 50 per cent acetone- METHODS water solution behind the knife edge and picked A tetraploid S. cerevisiae strain IF-5 was used up on formvar coated specimen grids. The sec- for the major part of this study, although some tions were drained on filter paper, air dried, and work was also done with a haploid strain. The selected for suitable thinness by their inter- tetraploid strain was chosen because of its larger ference colors when viewed under a direct size and because it had been studied cytologically illumination microscope at 80 X. The sections and genetically by other workers in this depart- were studied with an RCA model EMU-2b ment (Hawthorne, 1955). Vigorously budding electron microscope equipped with a self-biased cultures in the logarithmic phase were used. gun and a limiting aperture in the objective These were obtained by transferring cells to tubes pole piece to improve contrast. Electron micro- of broth (1 per cent yeast extract, 1 per cent graphs were taken at initial magnifications of peptone, 2 per cent glucose) from an overnight 3,800 X to 9,000 x with further photographic culture and incubating on a shaker at room enlargement as indicated. temperature for 4 to 6 hours. The cultures were Cell walls were prepared by disrupting yeast centrifuged and the supernatant discarded and suspensions in a Mickel tissue disintegrator, replaced by an osmium tetroxide fixative solu- followed by differential centrifugation and wash- tion. The 1.0 per cent buffered fixative of Palade ing. The cell walls were then fixed, dehydrated, (1952) and the fixative of Chapman and Hillier and embedded in methacrylate as described (1953) gave equally good results if the fixation above. time was prolonged to 16 to 20 hours. Osmium RESULTS AND DISCUSSION concentrations below 1 per cent and shorter A longitudinal section through a mother cell ' Supported in part by a grant from the State with two buds (A and B) at different stages of of Washington fund for Biological and Medical 2 Manufactured by Ivan Sorvall Inc., P.O. Box Research. 230, Pearl Street, Norwalk, Conn. 427 428 AGAR AND DOUGLAS [VOL. 70 Figure 1. Electron micrograph of a longitudinal section through a budding yeast cell. 14,000 X. A, bud with cytoplasm continuous with that of mother cell; B, mature bud with developing cross wall be- tween mother and daughter cell; C, bud scar; D, extension of cell wall material into cytoplasm. development is shown in figure 1. The cytoplasm pointed out below, this phenomenon appears to of bud A is still continuous with that of the be characteristic of the later stages of the budding mother cell, while in bud B the cytoplasmic con- process. A well-defined bud scar is present at C. tinuity no longer exists. The extension of cell In whole mounts of isolated cell walls, a bud scar wall material into the cytoplasm of the mother appears as a circular, raised rim on the surface cell and bud B is evident at D and, as will be of the cell wall (Northcote and Horne, 1952; u-Id .v #: 6. - Figure2.(lf)ntaino u fraina_ml ugei elwl.800X Fiue3(etr. Enagmn of cel walblet ml u.900X Fiur 4.l(rgt.Frhrelreeto u wt yols fmteagtern cel cotnos 8,000X.'S Figur5. Formto ofcl4almtra ymte n agtrcls 100X Fiue.Dobecrs wl bten~~~Figrsmohradduherclsna-oplto.900X 429 430 AGAR AND DOUGLAS [VOL. 70 ~~~~~~~~~~~~~~~~~~~~~~~~~. ::::..:.SA.::.'.. ...........:0':: . : : ; ; ::~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~.::: .: .: ...... :: .. S Ys~~~~~~~~~~~~~~~~~~~~ i.Sis.8. ...A.E- _ _ . ... .. s _ l~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~.......H _F .. ...;..._~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~. FigJiiie 7. Douible cross wsall eompletely formeJl s;howiii- the geometric fit of b)ud scar and b)irth scar. 38,00() X. Figiii-e 8. Siingle yeas;t (cll NAith b>irth seatr at upIper iiig,ht, alwl boud scarl at lowser left. 29,000 X. 1955] BUDDING AND CELL WALL STRUCTURE OF YEAST 431 Figure 9. Longitudinal section, shows lamellae of inner layer of cell wall. Figure 10. Longitudinal section, shows lamellae of the bud scar. 432 AGAR AND DOUGLAS [VOL. 70 Houwink and Kreger, 1953). The section through cytoplasm of the cells in figure 1 or the succeeding the scar at C shows the elevated edge of the rim figures. This is due to difficulties in sectioning and the enclosed, rounded plug of cell wall ma- which, in our experience, appear to be char- terial which forms the surface of the scar. The acteristic of yeast. In many cases the cytoplasm discontinuity in wall structure at the point of appears to be corrugated and somewhat com- contact of the plug and rim of the bud scar is also pressed. This "wash-boarding," caused ap- apparent. parently by internal chatter during cutting, Very little structural detail is evident in the makes difficult a study of structural detail in the .1 Figure 11. Electron micrograph of a longitudinal section through a yeast cell showing the electron dense fibrils lining inner surface of cell wall. 29,000 X. 19551 BUDDING AND CELL WALL STRUCTURE OF YEAST 433 Fig. 12. Electron micrographs of sectioned cell walls showing laminated structure of the wall. 28,000 X. cytoplasm. None of our sections have shown The precise manner in which the cell wall structures which could be identified as nuclei, separating mother and daughter cells is laid down vacuoles, or cytoplasmic granules, although their is not known, but our micrographs indicate that presence in the cells of strain IF-5 can easily be its formation might well resemble the pattern of demonstrated by other techniques. centripetal extension of the external cell wall that Figures 2 to 8 represent cells in different stages occurs in bacteria (Knaysi, 1941; Chapman and of bud formation. An early stage is seen in figure Hillier, 1953), with the essential difference being 2, where the bud is represented by a small bulge that new cell wall material may originate over a in the wall of the mother cell. A somewhat later much wider area. This is suggested by the ap- stage is presented in figure 3. In figure 4 the bud pearance of figures 5 and 6 described above, and is quite large but the cytoplasm of the two cells also by the structure of the bud scars. The plug is still continuous. The formation of the wall of cell wall material of the bud scar appears to which separates the cells is shown in figures 5 be attached to the inner side of the external cell and 6. In both figures there appears the char- wall over a considerable area (figures 1 and 10), acteristic extension of the cell wall material into and it may well be that the cell wall material of the cytoplasm which was noted previously in the plug originated over the entire area where figure 1. While it is difficult to interpret the plug and external wall are contiguous. significance of this phenomenon it appears to us With regard to the structure of bud and birth to represent a stage of active synthesis of the cell scars, our observations are in agreement with wall material, which eventually forms the convex those of Barton (1950), who first pointed out that and concave plugs of cell wall sealing the con- the two could be distinguished by their respective stricted opening between the cells. A cleavage convex and concave appearances. This was ques- line can be seen in the new cell wall material in tioned, however, by Bartholomew and Mittwer figure 6, while in figure 7 cleavage appears to be (1953), who found no difference in structure of complete and the geometric fit of the concave bud bud and birth scars of cells that had been treated scar and the convex birth scar is clearly demon- with ultraviolet light to make them more trans- strated. Figure 8 shows a single cell with a con- parent to the electron beam. cave birth scar at one pole and a convex bud scar The cell wall of S. cerevisiae is known to be a at the other.
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