Length control emerges from cytoskeletal network geometry

Abstract

Many cytoskeletal networks consist of individual filaments that are organized into elaborate higher order structures. While it is appreciated that the size and architecture of these networks are critical for their biological functions, much of the work investigating control over their assembly has focused on mechanisms that regulate the turnover of individual filaments through size-dependent feedback. Here, we propose a very different, feedback-independent mechanism to explain how yeast cells control the length of their actin cables. Our findings, supported by quantitative cell imaging and mathematical modeling, indicate that actin cable length control is an emergent property that arises from the cross-linked and bundled organization of the filaments within the cable. Using this model, we further dissect the mechanisms that allow cables to grow longer in larger cells, and propose that cell length-dependent tuning of formin activity allows cells to scale cable length with cell length. This mechanism is a significant departure from prior models of cytoskeletal filament length control and presents a new paradigm to consider how cells control the size, shape, and dynamics of higher order cytoskeletal structures. Significance StatementCells control the sizes of their cytoskeletal networks to ensure that these structures can efficiently perform their cellular functions. Until now, this ability has been attributed to molecular feedback mechanisms that control the rates at which individual filaments are assembled and disassembled. We find that size control of cytoskeletal networks does not require this type of feedback and can instead be encoded through the physical arrangement of the filaments within that network. These findings have important implications for understanding how the underlying geometry of higher order cytoskeletal networks contributes to cellular control over these structures.