The Limiting-Pool Mechanism Fails to Control the Size of Multiple Organelles

Abstract

How the size of micrometer-scale cellular structures such as the mitotic spindle, cytoskeletal filaments, the nucleus, the nucleolus, and other non-membrane bound organelles is controlled despite a constant turnover of their constituent parts is a central problem in biology. Experiments have implicated the limiting-pool mechanism: structures grow by stochastic addition of molecular subunits from a finite pool until the rates of subunit addition and removal are balanced, producing a structure of well-defined size. Here, we consider these dynamics when multiple filamentous structures are assembled stochastically from a shared pool of subunits. Using analytical calculations and computer simulations, we show that robust size control can be achieved only when a single filament is assembled. When multiple filaments compete for monomers, filament lengths exhibit large fluctuations. These results extend to three-dimensional structures and reveal the physical limitations of the limiting-pool mechanism of size control when multiple organelles are assembled from a shared pool of subunits.