Taking directions: the role of microtubule-bound nucleation in the self-organization of the plant cortical array

Abstract

The highly aligned cortical microtubule array of interphase plant cells is a key regulator of anisotropic cell expansion. Recent computational and analytical work has shown that the non-equilibrium self-organization of this structure can be understood on the basis of experimentally observed collisional interactions between dynamic microtubules attached to the plasma membrane. Most of these approaches assumed that new microtubules are homogeneously and isotropically nucleated on the cortical surface. Experimental evidence, however, shows that nucleation mostly occurs from other microtubules and under specific relative angles. Here, we investigate the impact of directed microtubule-bound nucleations on the alignment process using computer simulations. The results show that microtubule-bound nucleations can increase the degree of alignment achieved, decrease the timescale of the ordering process and widen the regime of dynamic parameters for which the system can self-organize. We establish that the major determinant of this effect is the degree of co-alignment of the nucleations with the parent microtubule. The specific role of sideways branching nucleations appears to allow stronger alignment while maintaining a measure of overall spatial homogeneity. Finally, we investigate the suggestion that observed persistent rotation of microtubule domains can be explained through a handedness bias in microtubule-bound nucleations, showing that this is possible only for an extreme bias and over a limited range of parameters.

Computer simulation and mathematical models of the noncentrosomal plant cortical microtubule cytoskeleton

“…The only scenario that resulted in consistent skewing without losing well-ordered CMT arrays was an abrupt switching from regular nucleation to branch-form nucleation after the formation of an ordered transverse array [Eren et al, 2010]. As mentioned above, Deinum et al [2011] simulated a related situation in which CMT nucleation continuously transitions from exclusively microtubule-independent to greater microtubule-dependent nucleation with increasing CMT density. This scenario did not result in array skewing in their simulations [Deinum et al, 2011].…”

“…As mentioned above, Deinum et al [2011] simulated a related situation in which CMT nucleation continuously transitions from exclusively microtubule-independent to greater microtubule-dependent nucleation with increasing CMT density. This scenario did not result in array skewing in their simulations [Deinum et al, 2011]. However, it is not easy to exactly compare these two studies as the nucleation scenarios, boundary conditions, and parameter ranges differ significantly between them.…”

“…Under these conditions, all CMT nucleations are microtubule-independent at the beginning of the simulations and the ratio of microtubule-dependent nucleation keeps increasing as the system becomes more crowded. Their results show that microtubule-dependent nucleation improves parallel CMT organization and widens the range of parameters for which organization occurs [Deinum et al, 2011]. In particular, they found parallel CMT nucleation to have a strong impact on CMT array organization.…”

“…[2010] discussed above. Deinum et al [2011] note that the main contribution of branchform nucleation was to result in spatially more homogeneous arrays than achieved by parallel nucleation alone. Together these findings are consistent with experimental observations which show that branch-form nucleation correlates with an increase in CMT spatial density and not parallel organization [Wasteneys and Williamson, 1989b].…”

“…A recent study by Deinum et al [2011] more completely analyzes the effects of branch-form nucleation on CMT organization by considering different branching processes and dynamicity parameters. In these simulations, CMT dynamicity is again limited to shortening-prone dynamics.…”