  Cell polarization underlies many cellular processes, such as differentiation,
migration, and budding. Many living cells, such as budding yeast and fission
yeast, use cytoskeletal structures to actively transport proteins to one
location on the membrane and create a high density spot of membrane-bound
proteins. Yet, the thermodynamic constraints on filament-based cell
polarization remain unknown. We show by mathematical modeling that cell
polarization requires detailed balance to be broken, and we quantify the
free-energy cost of maintaining a polarized state of the cell. Our study
reveals that detailed balance cannot only be broken via the active transport of
proteins along filaments, but also via a chemical modification cycle, allowing
detailed balance to be broken by the shuttling of proteins between the
filament, membrane, and cytosol. Our model thus shows that cell polarization
can be established via two distinct driving mechanisms, one based on active
transport and one based on non-equilibrium binding. Furthermore, the model
predicts that the driven binding process dissipates orders of magnitude less
free-energy than the transport-based process to create the same membrane spot.
Active transport along filaments may be sufficient to create a polarized
distribution of membrane-bound proteins, but an additional chemical
modification cycle of the proteins themselves is more efficient and less
sensitive to the physical exclusion of proteins on the transporting filaments,
providing insight in the design principles of the Pom1/Tea1/Tea4 system in
fission yeast and the Cdc42 system in budding yeast.
