Control of Flagellum Length by a Grow-and-lock Model

Several cell types such as photoreceptors and spermatozoa possess very stable cilia and flagella, a feature also encountered in numerous protists. We tested an original model for the control of flagellum length in such cells, using Trypanosoma brucei as an experimental system. The grow-and-lock model proposes that the flagellum elongates at a linear rate and that a locking event takes place in a timely defined manner preventing further elongation or shortening. We show that the total amount of IFT material increases during flagellum elongation, ensuring a constant concentration per unit of length and the ability to provide a constant delivery of precursors in agreement with a linear growth rate. Reducing the IFT rate by RNAi knockdown of the IFT kinesin motors slows down the growth rate and results in the assembly of shorter flagella. The flagellum is locked after cell division in an irreversible process and even subsequent increase in the IFT rate does not lead to further elongation. Other models (limitation by the soluble pool of tubulin, equilibrium between assembly and disassembly rates, or morphogenetic control) fail to explain the experimental data. The locking event is associated to the addition of the FLAM8 molecular marker at the distal end of the flagellum and is initiated prior cell division, leading to an arrest of elongation in the daughter cell. These results provide support for the grow-and-lock model as a new paradigm for the control of organelle length.