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Temperature-Sensitive Periods of Mutations J. Cell Set. 43, 59-74 (1980) Printed in Great Britain © Company of Biologists Limited igSo TEMPERATURE-SENSITIVE PERIODS OF MUTATIONS AFFECTING CELL DIVISION IN TETRAHYMENA THERMOPHILA JOSEPH FRANKEL,* JYM MOHLERf AND ANNE KOOPMANS FRANKEL Department of Zoology, University of Iowa, Iowa City, Iowa 52242, U.S.A. SUMMARY Temperature-sensitive periods were determined by application of temperature shifts and shocks to 3 temperature-sensitive cell division arrest (cda) mutants of Tetrahymena thermophila. A restrictive temperature, 36 °C, was found at which all 3 mutants are fully penetrant, yet other physiological effects are minimal. At this temperature, the temperature-sensitive period of cdaCl is a unique 5-min period in mid-division, that of cdaAi is a similarly brief period situated about 0-5 h prior to cell division, while the temperature-sensitive period of cdaHi is 20 to 30 min long and immediately precedes cell division. These periods either coincide with (cdaCi, cdaHi) or immediately precede (cdaAi) the onset of phenotypic abnormality at the restrictive temperature. Brief exposure to 36 °C during the temperature-sensitive period in any of these mutants brings about irreversible arrest of division furrows in progress or preparation. Mutant cells suffering such arrest can, however, divide again at a permissive temperature by forming new furrows at different sites. INTRODUCTION One major advantage of studying temperature-sensitive mutations affecting developmental processes is that such mutations invite the use of temperature treat- ments to find out the time at which gene products exert their phenotypic effects. Changes in temperature are used to demarcate a temperature-sensitive period (TSP) by 2 primary operations: shifts from restrictive to permissive temperature to delineate its beginning, and shifts from permissive to restrictive temperature to identify its end (Esposito, Esposito, Arnaud & Halvorson, 1970; Suzuki, 1970). A double-shift from permissive to restrictive temperature and then back again (i.e. a shock) may also be used to pinpoint TSPs (Poodry, Hall & Suzuki, 1973). Various combinations of these operations have been applied to characterize TSPs for expression of lethality, male sterility, and organ-specific defects in Drosophila (A. Frankel, 1973; Martin, Martin & Shearn, 1977; Shellenbarger & Mohler, 1978) as well as TSPs of mutants affecting starvation-mediated developmental sequences in the microorganisms Bacillus subtilis (Szulmajster, Bonamy & Laporte, 1970; Leighton, 1974; Young, • Author to whom reprint request should be sent. t Present address: Room 16-720, Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, U.S.A. 5-2 60 J. Frankel, J. Mohler and A. K. Frankel 1976; Sumida-Yasumoto & Doi, 1977) and Saccharomyces cerevisiae (Esposito et al. 1970). With one recent exception (Melero, 1979), studies on the effects of temperature- sensitive (TS) mutations on the eukaryotic cell cycle have employed only shifts from permissive to restrictive temperature, and used these to characterize an 'execution point', defined as '.. .the time in the cell division cycle when the temperature- sensitive gene product completes its function at the permissive temperature' (Hart- well, 1971a) [also termed 'block point' (Howell & Naliboff, 1973); 'transition point' (Nurse, Thuriaux & Nasmyth, 1976) and 'shift-up point' (Ashihara, Chang & Baserga, 1978)].* This defines the end of the TSP. Execution points have been determined for a large number of TS cell division cycle mutants in Saccharomyces (Hartwell, Mortimer, Culotti & Culotti, 1973), Schizosaccharomyces (Nurse et al. 1976), Aspergillus (Orr & Rosenberger, 1976), and Chlamydomonas (Howell & Naliboff, 1973) and also for G1-arrest mutations in mammalian cell lines (Ashihara et al. 1978; Melero, 1979). TS mutations at 7 loci that bring about arrest at specific stages of cell division in the ciliate Tetrahymena thermophila (formerly T. pyriformis syngen 1) have been characterized genetically (Frankel, Jenkins, Doerder & Nelsen, 19766; Jenkins, un- published) and phenotypically (Frankel, Jenkins & DeBault, 1976 a; Frankel, Nelsen & Jenkins, 1977; Cleffrnann & Frankel, 1978; Frankel, unpublished). At 3 of these loci, cdaA, cdaC and cdaH, mutant alleles are available that bring about 100% arrest within the first cycle after the shift to restrictive temperature, and are therefore well suited for analysis of TSPs. The present communication is an analysis of the TSPs of mutations at these 3 loci, and also includes a demonstration of the local irreversibility of effects incurred during these TSPs. MATERIALS AND METHODS Stocks and media All cells used in this study were of inbred strain B of Tetrahymena thermophila. The strain B was obtained from. Dr D. L. Nanney in 1972, when in its 18th generation of inbreeding. It was inbred a 19th time in our laboratory in 1975, and designated B-1975. A single wild type stock, of mating type II, was used. Four mutant stocks, homozygous for each of 3 TS cda (cell division arrest) genes, were employed. cdaAl (formerly moi") and cdaCz (formerly motf) were each represented by a single homozygous stock, IA-105 (mating type III) for the former and IA-123 (m.t. VII) for the latter. Two stocks homozygous for cdaHl were used: IA-150 (m.t. V) for analysis of silver-impregnated slides and furrowing times and IA-149 (m.t. II) for the remainder of the single-cell work. We will refer to stocks by the mutant alleles that they carry as homozygotes. The culture medium generally utilized contained 1 % proteose peptone plus o-i % Difco Bacto yeast extract (1 % PPY). • We will continue to use 'execution point' as a synonym for the end of the TSP. Of the alternative expressions, 'block point' invites confusion between the end of the TSP and the time of phenotypic expression, while 'transition point' creates a potential for confusion between the ends of gene-specific TSPs and the more general 'physiological transition point' (c.f. Frankel, Mohler & Frankel, 1980). Temperature-sensitive periods of Tetrahymena mutations 61 Single-cell procedures Fifty- to 150-ml batches of medium in 250-ml conical flasks or 500-ml Fernbach flasks were inoculated at roughly 10 cells/ml from a 2-day-old tube culture and preincubated at 25 °C without shaking or aeration for about 20 h, to attain a density of about 1000 cells per ml when experiments were begun. A small portion of this culture was poured out into a glass Petri plate, for selection of single cells. In most experiments, the drop-culture procedure of Lovlie (1963) was used. Single non-dividing cells were selected at random and deposited in small drops of culture medium on the surface of plastic Petri dishes (Falcon no. 1008 or 3005), 25 drops to a dish. The drops were covered with a thin layer of light paraffin oil (viscosity 125/135) and maintained at 25 ± 1 °C. These drop cultures were examined at io-min intervals under a dissecting microscope and the state of cells with respect to cell division was noted. Cell divisions completed in each interval were recorded. After all cells in a newly established culture dish had divided, the dish, containing individually cultured pairs of sister cells of known interfission ages, was transferred to a waterbath set at a temperature ranging from 36'0 to 400 °C, according to the experiment. The temperatures in the drops were recorded using a thermistor probe connected to a tele-thermometer (Yellow Springs, model 47). The equilibrium temperature in the drop-cultures, about 1 -o °C below the bath temperature, was reached within 5 min after transfer. In the shift-up experiments, the culture dishes were re- moved from the waterbath after 3 h at the high temperature and scored as to whether or not a second division had taken place. In the shock experiments, the culture dishes were kept at the restrictive temperature for only 20 min, and then returned to 25 CC. They were observed under the dissecting microscope immediately after removal from the high temperature bath, and at io-min intervals thereafter. Calculation of the generation time of each cell was based on the total time elapsed between the completion of one division and that of the next, accurate to within ± 5 min. A variant of the above procedure was employed in shift-down experiments. Dividing cells were selected and placed in individual micro-drops. The exact time of division of these cells was recorded, and the culture dish was transferred to the waterbath, set 1 °C above the desired restrictive temperature, immediately after the division of the last cell (and within 10 min of the division of the first). The cells were kept at the high temperature for 70 min or more, and then removed from the bath and observed at frequent intervals at 25 °C to find out whether or not the subsequent division was successfully completed. In most experiments, one dish with mutant cells was maintained continuously at 25 CC, as a control, while other dishes of the same culture were given concurrent shocks or shifts. In certain experiments, wild-type cells were studied simultaneously with mutants in a 2x2 experimental design (wild type and mutant, each at 25 and 36 °C). In the culture-dish experiments, all cells were observed during the 2-3 min preceding the shift to high temperature, and, where possible, were classified according to visible stages related to cell division. The process of division furrowing (cytokinesis) was arbitrarily categorized into 5 stages, and one stage just prior to cytokinesis (B) could also be recognized. The B stage is characterized by a semi-rectangular (or 'boxy') shape, the E stage by a 'notch' on one side, the MB stage by a complete furrow less than one-third of the cell diameter deep, the M stage by a furrow one- to two-thirds of the cell diameter deep, the ML stage by a furrow more than two-thirds of the cell diameter deep but with a distinct waist still present, and the L stage by a figure-eight appearance with a waist of no distinguishable thickness as observed at 40 x magnification.
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