Robust banded protoxylem pattern formation through microtubule-based directional ROP diffusion restriction

Bas Jacobs,Jaap Molenaar,Eva E Deinum

doi:10.1016/j.jtbi.2020.110351

Abstract

In plant vascular tissue development, different cell wall patterns are formed, offering different mechanical properties optimised for different growth stages. Critical in these patterning processes are Rho of Plants (ROP) proteins, a class of evolutionarily conserved small GTPase proteins responsible for local membrane domain formation in many organisms. While te spotted metaxylem pattern can easily be understood as a result of a Turing-style reaction-diffusion mechanism, it remains an open question how the consistent orientation of evenly spaced bands and spirals as found in protoxylem is achieved. We hypothesise that this orientation results from an interaction between ROPs and an array of transversely oriented cortical microtubules that acts as a directional diffusion barrier. Here, we explore this hypothesis using partial differential equation models with anisotropic ROP diffusion and show that a horizontal microtubule array acting as a vertical diffusion barrier to active ROP can yield a horizontally banded ROP pattern. We then study the underlying mechanism in more detail, finding that it can only orient curved pattern features but not straight lines. This implies that, once formed, banded and spiral patterns cannot be reoriented by this mechanism. Finally, we observe that ROPs and microtubules together only form ultimately static patterns if the interaction is implemented with sufficient biological realism.

Highlights

Plants are able to transport water and nutrients from the ground all the way up to the leaves, potentially more than a hundred meters high, thanks to a highly specialised system of vessels known as the xylem (Brown, 2013)
Increasing the ROP production rate or the total amount of ROP changes the native pattern from spots to stripes to gaps (Jacobs et al, 2019), a sequence of patterns often observed in similar models (Meinhardt, 1952)
We have shown that restricting active ROP diffusion in a specific direction is sufficient to change the output from a ROP-based Turing-style pattern formation mechanism from patterns without specific orientation into banded or spiral patterns with controlled orientation

Summary

Introduction

Plants are able to transport water and nutrients from the ground all the way up to the leaves, potentially more than a hundred meters high, thanks to a highly specialised system of vessels known as the xylem (Brown, 2013). The secondary wall forms bands or spirals, allowing the vessels to stretch with the surrounding tissue, while metaxylem, formed when longitudinal tissue growth has ceased, tends to be more rigid, with only some well-separated pits for radial transport (Oda and Fukuda, 2012a; Sperry et al, 2003; Choat et al, 2008) (Fig. 1A). The deposition of this secondary cell wall is determined by the position of cortical microtubules on the inside of the membrane that direct cell wall depositing cellulose synthase complexes. Since ROP involvement has been indicated in protoxylem differentiation (Brembu et al, 2005) and the same effectors (MIDD1, Kinesin13A) are expressed during protoxylem development (Yamaguchi et al, 2011; Brady et al, 2007), patterning of protoxylem is expected to have a similar mechanism to that of metaxylem

Methods

Results

Conclusion