Deborah Shelton and colleagues have published a new article arguing that the reigning model of cell division initiation in Chlamydomonas reinhardtii needs to be revised [full disclosure: Dr. Shelton and I were labmates in Rick Michod’s lab at the University of Arizona]. The evolution of multicellularity almost certainly involved changes in cell cycle regulation; for example, there is good evidence that changes to the cell cycle regulator retinoblastoma were involved in the initial transition to multicellular life in the volvocine algae. So understanding cell cycle regulation is vital for understanding the evolution of multicellularity.
Chlamydomonas, and in fact nearly all volvocine algae, have an unusual pattern of cell division:
Many organisms used to study the cell cycle undergo only one division during the division phase, producing two equally-sized offspring, a type of cycle known as binary fission. By contrast, C. reinhardtii…has an asexual cell division cycle in which an extended growth period (G1) is interspersed with a series of n rapid rounds of division (where n is an integer, generally between 1 and 5, and 2n equally-sized offspring result).
In other words, Chlamydomonas cells, instead of doubling in size and then dividing, grow to many times their original size and then quickly divide up to five times, with little or no growth between rounds of cell division. The cells of most multicellular volvocine algae do the same thing, and the number of cell divisions determines the number of cells in the offspring colonies (for example, an n of 6 produces 64-celled colonies).
Since the 1980s, the consensus view has been that Chlamydomonas division is controlled by a ‘sizer’ and a ‘timer’: cells commit to dividing when they reach a certain size (the sizer) and begin dividing a (more or less) fixed time later (the timer):
This model does a good job of describing the growth and reproduction of Chlamydomonas cells grown under continuous light, but problems begin to appear when darkness falls during the timer delay. Once cells have reached the commitment size, the model predicts that they should begin dividing at the same time (i.e. 5-10 hours later) regardless of whether or not they continue to be exposed to light. Cells growing under continuous light should get bigger than those moved to the dark (because they continue to photosynthesize and grow), and might therefore undergo more divisions once the timer has expired, but when they start dividing shouldn’t depend on the post-commitment light conditions. And this is contradicted by several experiments that show that post-commitment light conditions do affect the timing of the first cell division.
To account for this discrepancy, Shelton and colleagues propose an alternative model with an additional decision:
Instead of dividing a fixed time after the commitment size is reached, cells divide when they either reach a growth-rate dependent target size (in the light) or in the dark when there are other indications that it is night. Those other indications might include
…things like a prolonged period of dark or a period of dark that immediately follows a period of reddish light (i.e., the color profile indicative of dusk).
The proposed model is an attempt to account for observed differences in the timing of division initiation under different post-commitment light conditions. Aside from the presence or absence of light, the color of light has also been shown to affect this timing. Although it is a bit more complicated, the new model seems to be a better fit to experimental data (and the paper includes a discussion of the relative merits of parsimony and consistency with observations).
The authors are clear that the proposed model is a hypothesis to be tested rather than the final word and that “new data…are needed to definitively characterize cell behavior.” But it is clear that some modification to the traditional model is needed to account for the observed behavior of cells. Modifications of the sizer/timer model have been proposed to explain differences in cell number among multicellular volvocine algae (Koufopanou 1994), so understanding the factors that control cell division may help to explain aspects of multicellular development. In addition to the new data on Chlamydomonas that Shelton and colleagues call for, experiments aimed at understanding cell cycle control in various volvocine species could shed light on the evolution of multicellularity.
Koufopanou, V. 1994. The evolution of soma in the Volvocales. Am. Nat. 143:907–931.
Shelton, D. E., M. Leslie, and R. E. Michod. 2016. Models of cell division initiation in Chlamydomonas: a challenge to the consensus view. J. Theor. Biol. 412:186–197.