A new method of determining the dependence of cell growth on the initial cell volume in the absence of cell division is presented. The assumptions are that volume in a certain period of time is either increasing or decreasing, but not both, and is independent of the history of cells. Applying this method to Gonyaulax polyedra in a 12h light-12h dark cycle, growth in volume between the 3rd and 12th hours of the light period is found to be more exponential-like than linear. The magnitude of growth in the time period is determined solely by cell volume and environmental conditions, not by cell age. All cells decrease in volume slightly in the dark from the 12th to 23rd hour, and then increase a little from the 23rd to 3rd hour of the following day. Cell division in this species is significantly asymmetric, and the extent of asymmetry is estimated mathematically. Simulations based on the growth patterns and the asymmetric division reveal that cell division must at least partly depend on the volume of cells. The dependence of conditional cell division probability on cell volume is then experimentally determined. The probability is zero up to a certain cell volume, and then it gradually increases to a plateau level, which is less than unity. Neither the strict size control model nor the transition probability model is fully consistent with the observed shape of the conditional probability function. A hybrid model postulating a ‘sloppy’ critical volume with a constant probability of division above that volume adequately accounts for the conditional probability. With the use of the observed volume growth law, cell division dependence on volume, and the extent of asymmetry in cell division, cell volume distributions are successfully simulated for cells growing in a 12h light-12h dark cycle. Another simulation reveals that the true coefficient of variation in generation time is 33%. On the basis of these findings, a model of the cell cycle is presented that incorporates the circadian clock as a cyclic G1 phase. According to this scheme, cells satisfying the minimum cell volume requirement between the 12th and the 18th hour probably exit to the replication/segregation sequence ending in division, and re-enter the cyclic portion after a fixed time interval.

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