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Ascospore Development in the Fission Yeasts Schizosaccharomyces Pombe and S. Japonicus

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Ascospore Development in the Fission Yeasts Schizosaccharomyces Pombe and S. Japonicus J. Cell Sd. 56, 263-279 (1982) 263 Printed in Great Britain © Company of Biologists Limited 1982 ASCOSPORE DEVELOPMENT IN THE FISSION YEASTS SCHIZOSACCHAROMYCES POMBE AND S. JAPONICUS KENJI TANAKA* AND AIKO HIRATA Institute of Applied Microbiology, The University of Tokyo, Bunkyo-ku, Tokyo 113, Japan SUMMARY The fine structure of ascospore formation in the fission yeasts Schizosaccharomyces pombe and Schizosaccharomyces japonicus var. japonicus was studied by serial thin-sectioning and electron microscopy. The morphogenetic events were almost the same in both species. Ascospore development was initiated by the formation of the forespore membrane on the cytoplasmic side of the differentiated nucleus-associated organelle (NAO) in the interval between meiosis I and II in S. pombe, or during the post-meiotic nuclear division in S. japonicus, and the process proceeded almost synchronously through the two or four nuclei in the ascus. The forespore membrane developed by fusion of the cytoplasmic vesicles and this was clearly demonstrated in S. japonicus where the behaviour of vesicles involved in the forespore membrane development could be traced as they were marked by the presence of electron-dense granules. The staining technique, by phosphotungustic acid-chromic acid (PTA-CA) after treatment with periodic acid, was used to attempt to elucidate the origin and the nature of the forespore membrane. The method specific to plasmalemma-type membranes stained both ascus and ascospore plasmalemmas; the forespore membrane was not stained at first but developed the same affinity for stain as the plasma membrane in the course of ascospore development. The results suggest that the forespore membrane did not come directly from the ascus plasma membrane, but from another membrane system such as the endoplasmic reticulum. Spore wall material was deposited in the space between the inner and outer leaflets of the forespore membrane. INTRODUCTION Ascospore development in yeasts seems to be one of the most advantageous systems for the study of cell differentiation. Ascospore formation in bakers' yeast involves zygote formation by conjugation between sexually compatible cells, meiotic divisions and ascospore development in the ascus. Ascospore delimitation in Saccharomyces cerevisiae has been observed to be initiated at the site of spindle-pole bodies or nucleus-associated organelles (NAOs) of the second meiotic spindles, by the develop- ment of a pair of unit membranes (Moens & Rapport, 1971; Peterson, Gray & Ris, 1972), between which the spore wall is subsequently laid down (Lynn & Magee, 1970; Beckett, Illingworth & Rose, 1973). However, the origin of the ascospore- delimiting membrane has not been clarified. • Present address: Institute of Medical Mycology, Nagoya University School of Medicine, Showa-ku, Nagoya 466, Japan. 264 K. Tanaka and A. Hirata The fission yeast Schizosaccharomyces pombe has been used widely for cell-cycle and genetic studies, and the ultrastructure of ascospore formation also has been studied by several investigators (Conti & Naylor, i960; Yoo, Calleja & Johnson, 1973). They have established the basic outline of events in the process leading to the formation of ascospores, but have not revealed any details of the nuclear structures in the process, because they used fixation with permanganate exclusively for studies of the membrane structures. Olson, Eden, Egel-Mitani & Egel (1978) have provided electron micrographs of sections of S. pombe nuclei undergoing meiosis. Our own experience of early phases of this process has been similar (Hirata & Tanaka, 1982) and the conclusions have been incorporated into Fig. 1. This paper describes the ultrastructural details of the origin and formation of the ascospore-delimiting membranes of glutaraldehyde-osmium tetroxide fixed cells during ascosporogenesis in S. pombe and in Schizosaccharomyces japonicus var. japonicus as demonstrated by serial thin-sectioning and electron microscopy. MATERIALS AND METHODS Organisms and culture for sporulation S. pombe strain I190 a homothallic strain and S. japonicus Yukawa et Maki var. japonicus IFO 1713 were used in this study. For the sporulation of S. pombe, cells were cultured in presporulation medium, which contained 3 % glucose and 0-5 % yeast extract, and harvested at the early stationary phase of growth. After washing once in distilled water, cells were inoculated into 100 ml of sporulation medium (SSL) in conical flasks at a density of about 5 x 10' cells per ml (Egel, 1971). They were shaken at 30 °C. In these conditions sporulation was completed within 24 h. Sporulation of S. japonicus was brought about by following the method described by Tsuboi, Ohashi, Takahara & Hayashibe (1978). Modified Burkholder medium (B medium) supplemented with 0^5 % yeast extract and 0-5 % malt extract (BYM medium) was prepared for the presporulation culture, which was kept in the dark to avoid light-induced sexual flocculation. Sporulation was carried out in B medium, from which (NH4),SO4 was omitted (B — N medium), in the light with shaking, at 26 °C. Electron microscopy For electron microscopy aliquots were taken at intervals from the sporulation culture, and cvi vol. of glutaraldehyde fixative was added before centrifugation. Centrifuged cells were resuspended in fresh fixative at room temperature for 2 to 3 h, and then stored in a refrigerator. The fixative was a 3 % glutaraldehyde solution in potassium phosphate buffer (pH 7-0). Fixed Fig. 1. A diagrammatic representation of meiosis and the development of ascospores in S. pombe and S. japonicus var. japonicus. A to D are common to the two species. A. A zygote with two nuclei (dotted), each associated with a single NAO. B. Fusion of the two nuclei is preceded by fusion of both NAOs. c. A fused and elongated nucleus, with a fused NAO at one end containing a number of linear elements, which is thought to be a stage of meiotic prophase. D. Meiosis I nucleus with a spindle (parallel lines) between a pair of NAOs. E and F, from S. pombe. E. Forespore membranes of double membrane sacs originating on the cytoplasmic sides of the NAOs cover the half-spindles of meiosis II in the two nuclei. F. Four ascospores with thick walls. Spore nuclei carry their respective NAOs. c, H and 1, from S. japonicus. c. Two nuclei with spindles at meiosis II in the ascus. H. Forespore membranes developing on the differentiated NAOs of the post-meiotic spindles of four nuclei. Development seems to proceed synchronously through the four nuclei. 1. An eight-ascospore ascus. Ascospore development in fission yeast 265 A Fig. 1 266 K. Tanaka and A. Hirata or fm V. 30L1 '•% c Ascospore development in fission yeast 267 cells were washed several times in buffer, and treated with Zymolyase 60000 (Kirin Brewery Co. Ltd, Takasaki, Japan) (o-i mg/ml) in the same buffer at 30 °C. The disintegration of the cell wall was examined with a phase-contrast microscope. The Zymolyase-treated cells were washed again in buffer and postfixed in 2 % OsO4 for 2 h at room temperature. After washing in distilled water, they were soaked in a 0-5 % (w/v) aqueous solution of uranyl acetate for 2 h and embedded in agar blocks. The cells were dehydrated by passing them through a series of increasing concentrations of ethanol and absolute acetone, and then they were embedded in Spurr's resin. Serial sections were obtained with a Dupont diamond knife on a Porter- Blum MT-2 ultramicrotome and treated by one of the following methods. (1) Sections were mounted on Formvar-coated single-slot grids and stained with uranyl acetate and lead citrate. (2) In order to apply specific staining to the plasmalemma, sections were collected using a small plastic sheet with a hole (3-0 mm diameter) punched through it at one end. Sections floating on a film of distilled water within the hole were treated with 1 % periodic acid and stained with phosphotungustic acid plus chromic acid (PTA-CA) (Roland, Lembi & Morr6, 1972). Sections were viewed with a JEOL 200 CX electron microscope at 100 kV. RESULTS Ascospore formation in the fission yeast involves the developmental stages of cell flocculation, cell fusion, karyogany, meiotic nuclear divisions, ascospore delimitation by the development of double unit membranes or forespore membrane, and spore wall maturation. The morphological changes in the meiotic nuclei and the process leading to ascospore formation were almost the. same in 5. pombe (Hirata & Tanaka, 1982) and S. japonicus (Hirata & Tanaka, unpublished observations), except that the latter underwent one additional nuclear division before ascospore delimitation began. This is illustrated in Fig. 1. Conjugation of the two haploid cells resulted in a binucleate zygote (A) where karyogamy had occurred by fusion of the two nucleus-associated organelles (NAOs) (B). At the presumed prophase in meiosis I, the zygote nucleus with a fused NAO at one end was elongated and contained a number of filamentous linear elements (c) (Olson et al. 1978). Nuclear division was effected by a spindle consisting of microtubules connecting NAOs at opposite poles (D). In 5. pombe ascospore delimitation first became apparent at the start of meiosis II (E) and a four-spored ascus was produced (F). In 5. japonicus this event is delayed because in this species meiosis is followed by another round of nuclear division (G, H). The primary envelopes for the eight spores about to be created begin to be formed simultaneously near the NAOs at the spindle poles of the dividing haploid nuclei even before these mitoses have been completed (H, I). Figs. 2-10. S. pombe. Fig. 2. A zygote at meiosis II. Two nuclei that are the products of meiosis I seem to be at almost the same stage of meiotic division as shown by the presence of spindle microtubules (arrow). This indicates that meiosis II is proceeding syn- chronously between the two nuclei, x 16coo. Fig. 3. Two consecutive sections (A, B) show the multi-plaque structure of the modified NAO (nao) at meiosis II and the forespore membrane (fin) developing on it.
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