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A Mutant of Tetrahymena Thermophila with a Partial Mirror-Image Duplication of Cell Surface Pattern

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A Mutant of Tetrahymena Thermophila with a Partial Mirror-Image Duplication of Cell Surface Pattern /. Embryol exp. Morph. Vol. 49, pp. 167-202, 1979 Printed in Great Britain © Company of Biologists Limited 1979 A mutant of Tetrahymena thermophila with a partial mirror-image duplication of cell surface pattern I. Analysis of the phenotype By MARIA JERKA-DZIADOSZ1 AND JOSEPH FRANKEL2 From the Department of Zoology, University of Iowa SUMMARY Cells of a mutant clone, CU-127, of Tetrahymena thermophila (formerly T. pyriformis, syngen 1) manifest three anatomical abnormalities. First, the stable number of ciliary meridians is 21-25, above the usual number (17-21) in this species. Second, up to 30 % of the cells have two oral apparatuses (OAs), one normal and the other abnormal. Third, more than one-half of the cells possess two distinct sets of contractile vacuole pores (CVPs). In some living cells two contractile vacuoles are seen. These abnormalities have persisted un- changed during more than 500 generations of vegetative propagation, and are similarly expressed in subclones. The normal and abnormal OAs are topographically segregated, with normal OAs developing along the 'primary oral axis' and abnormal OAs developing along a 'secondary oral axis' that is situated 170° of the cell circumference to the cell's right of the primary oral axis. CVPs always appear within this 170° arc and never within the com- plementary 190° arc to the left of the primary oral axis. A unique feature of the CU-127 clone is the commonly expressed mirror image reversal of the structural pattern of OAs that develop along the secondary oral axis. The primordia of such OAs initially appear (as usual) to the cell's left of a ciliary meridian, but as membranelles develop they frequently come to be oriented in a mirror image of the normal pattern, and an undulating membrane sometimes develops on the wrong (left) side of the oral primordium. When two sets of CVPs are formed, their average positions are roughly equidistant with respect to the two oral axes, with the two sets located 50-60° to the right and left respectively of the primary and secondary oral axes. Such cells are thus bilaterally symmetrical about a plane defined by the central longitudinal axis and the halfway point between the two CVP sets (see Fig. 25). This plane bisects the cell into a normal and a 'reversed' half-cell. However, only oral asymmetry and large-scale CVP positioning are subject to such reversal; all ciliary meridians remain of normal asymmetry and all CVPs are situated on the left side of CVP meridians. The fact that major aspects of large-scale cellular organization can be reversed while the 'fine-positioning' associated with the ciliary meridians remains normal indicates that the two aspects of cell organization are distinct. 1 Author's address: Department of Cell Biology, M. Nencki Institute of Experimental Biology, Pasteura 3, Warsaw 02-093, Poland. 2 Author's address (for reprints): Department of Zoology, University of Iowa, Iowa City, Iowa 52242, U.S.A. 168 M. JERKA-DZIADOSZ AND J. FRANKEL INTRODUCTION Positioning of cell surface organelle systems in ciliated protozoa involves interactions taking place over very small as well as relatively large intracellular distances. There has been considerable discussion in the literature over the degree to which the mechanisms governing long-range positioning differ from those controlling short-range positioning (Frankel, 1974, 1975; Jerka-Dziadosz, 1974; Lynn & Tucker, 1976; Lynn, 1977; Sonneborn, 1975). The paradigm for short-range positional interactions is the propagation of the ciliary meridian. Within this ensemble new structures such as basal bodies and accessory fibrillar and microtubular systems are positioned in definite spatial relations to nearby pre-existing structures. The proof of the determinative role of the pre-existing topographic arrangement within ciliary meridians was the demonstration that an 180° inversion of that arrangement is faithfully propagated. This was shown first in Paramecium (Beisson & Sonneborn, 1965) and later in Tetrahymena (Ng & Frankel, 1977; Ng & R. Williams, 1977). In Tetrahymena it was further ascertained that the geometry of the ciliary meridian also controls the fine- positioning of the contractile vacuole pore (Ng, 1977, 1978) as well as aspects of the positioning of cortically situated mitochondria (Aufderheide, 1978). Investigation of positioning of structures such as new oral apparatuses has been carried out mainly by microsurgical experiments on large ciliates, such as Stentor (Tartar, 1962; Uhlig, 1960) and urostylids (Jerka-Dziadosz, 1974, 1977). The results of these experiments suggest that positioning over long intracellular distances may involve 'gradient-fields' that may be analogous to those operating in multicellular development (Frankel, 1974, 1975; Jerka-Dziadosz, 1974). In Tetrahymena, morphometric analyses of the cell latitudes at which new oral apparatuses are formed (Lynn & Tucker, 1976; Lynn, 1977) and of the longitudes at which new contractile vacuole pores appear (Nanney, 1966 a) suggest that both structures are determined relationally as joint functions of reference points (or axes) and aspects of overall cell size. A decisive judgement of the relationship of long-range positioning systems to the better-understood short-range systems could be made if it were possible to rotate or reverse either system within the spatial domain of another. One way of doing this would be to obtain a propagated geometrical reversal of some aspect of large-scale cellular organization. A propagated reversal of asymmetry of feeding structures has already been obtained in mirror-image doublets of hypotrich ciliates (Faure-Fremiet, 1945; Tchang, Shi & Pang, 1964; Tchang & Pang, 1965; Dryl & Totwen-Nowakowska, 1972), but these cases have not been subjected to detailed cytological analysis. Recently, however, we have encountered a clone of Tetrahymena thermophila that indefinitely perpetuates the capacity to manifest a mirror-image reversal of oral structures at a well- defined cellular position and also maintains a corresponding reversal of con- tractile vacuole pore positions. Since in Tetrahymena (unlike the hypotrichs Mirror-image duplication in Tetrahymena 169 referred to above) both oral structures and contractile vacuole pores develop in the close neighborhood of ciliary meridians (reviewed in Frankel & Williams, 1973), this reversal achieves the desired superimposition of two positional systems. The cytological analysis to be presented here shows that these two systems are indeed separate and dissociable. The accompanying paper (Frankel & Jenkins, 1979) demonstrates that the unique reversal of asymmetry in this clone is under genie control, and provides further evidence for the separation of short-range and long-range positional controls. MATERIALS AND METHODS The CU-127 clone of Tetrahymena thermophila (Nanney & McCoy, 1976) that is the subject of this investigation was obtained in December 1976 from the laboratory of Dr P. Bruns. It had previously been subjected to mutagenesis in 10 /Ag/ml of iV-methyl-A^'-nitrosoguanidine, followed by short-circuit genomic exclusion, a protocol designed to select homozygous cells rapidly (Bruns, Brussard & Kavka, 1976). CU-127 was one of a subset of morphologically abnormal clones among a larger number of clones that had been screened for temperature sensitivity following the above-mentioned mutagenesis and genomic exclusion protocol (Bruns & Sanford, 1978). All but one of the experiments were performed on a sample received directly from Dr Bruns' laboratory in December 1976. One experiment (cf. Table 6; Table 7, II) was carried out on another sample that had first been sent by Dr Bruns to Dr D. L. Nanney's laboratory for cryo- preservation and was received from there in February 1977; this is designated CU-127 (111.). The media used in experiments were all axenic, and consist of four different recipes: TGVS: 0-3% bacto-tryptone (Difco), 0-5% glucose, vitamins, and salts (Frankel, 1965); 1 % PPY: 1 % proteose peptone (Difco) plus 01 % yeast extract (Difco); 2 % PPY: 2 % proteose peptone plus 0-5 % yeast extract; Dryl's: Dryl's inorganic medium made up as described by Nelsen & DeBault (1978). Stocks were maintained at 28 °C in axenic tube cultures containing 5 ml of 1 % PPY or TGVS medium, with transfer daily or every second day [weekly for CU-127 (111.)]. Fernbach flasks (500 ml, Jena Glaswerk) containing 100 ml of medium were inoculated with one to five drops of 1-day-old tube culture. Flasks containing TGVS medium were inoculated with cells from TGVS tubes, while flasks with 1 % PPY or 2 % PPY medium were inoculated from 1 % PPY tubes. The flask cultures were incubated for 20-24 h at 28° ± 1 °C to yield mid-log phase cultures (cell density 15000-50000 per ml). In some cases such cultures were shifted to a bath set at 40° ±0-1 °C (39-5 °C inside flask) and maintained at that temperature for various durations (usually 4-5-5 h), following which, in certain experiments, the flask was returned to 28 °C for 1-5 h. Samples were fixed at various intervals. In a few experiments cultures were fixed after being allowed to enter stationary 170 M. JERKA-DZIADOSZ AND J. FRANKEL phase by 48 h continuous maintenance at 28 °C, or by 24 h following a shift of a mid-log phase culture from 28 to 40 °C. In still other experiments, cells grown in 1 % PPY at 28 °C were washed by centrifugation and transferred to Dryl's inorganic medium and maintained under various temperature regimens. In one experiment, the cells were maintained in 1 % PPY and TGVS tubes, with daily transfer, for 10 successive days at 39-5 °C. After the tenth such serial tube-culture had reached late-log phase, the contents of the entire tube were poured into a Fernbach flask containing 100 ml of medium, kept at 39-5 °C for 3 h, and fixed. These cultures had thus spent about 100 cell generations at 39-5 °C prior to fixation. In another experiment, a CU-127 culture growing in 1 % PPY was subjected to clonal expansion.
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