Branching, crosslinking and decentralization of microtubules accelerates intracellular assembly

Before cell division, mitotic spindle is assembled from chromosomes and centrosomes. After the cell division, Golgi organelles assemble from multiple vesicles scattered across daughter cells. These are among many other examples of intracellular assembly of vesicles, organelles and chromosomes made possible by dynamic microtubules. The most prominent microtubule networks are centrosome-focused asters that ‘search’ for the vesicles and chromosomes, but there are also microtubules originating from the vesicles and chromosomes, raising the question whether a coordination between multiple microtubule networks optimizes the assembly process. This study uses a computational model to examine how microtubule dynamics influence the assembly of organelles from vesicles. The model includes two microtubule populations: microtubules anchored to the vesicles, which drive local clustering, and ‘central’ microtubules anchored to the centrosome that aggregate the vesicles globally. Simulations show that a microtubule decentralization – balanced contribution from both microtubule populations — accelerates the assembly of tens of vesicles, but that assigning all microtubules to hundreds of vesicles optimizes the assembly. Directionally biased microtubule growth, particularly when avoiding spontaneous catastrophe events, further accelerates the assembly. Additionally, microtubule branching, when occurring at optimal angles and spacings, enhances the assembly’s efficiency. Lastly, rapid crosslinking of overlapping central and ‘local’ microtubules can drastically accelerate the assembly. Applying this model to the spindle assembly in early mitosis reveals similar insights. The model suggests that the observed multiple microtubule networks optimize the intracellular assembly processes when molecular resources are limited.