Abstract

BackgroundLocal activation of Rho GTPases is important for many functions including cell polarity, morphology, movement, and growth. Although a number of molecules affecting Rho-of-Plants small GTPase (ROP) signalling are known, it remains unclear how ROP activity becomes spatially organised. Arabidopsis root hair cells produce patches of ROP at consistent and predictable subcellular locations, where root hair growth subsequently occurs.Methodology/Principal FindingsWe present a mathematical model to show how interaction of the plant hormone auxin with ROPs could spontaneously lead to localised patches of active ROP via a Turing or Turing-like mechanism. Our results suggest that correct positioning of the ROP patch depends on the cell length, low diffusion of active ROP, a gradient in auxin concentration, and ROP levels. Our theory provides a unique explanation linking the molecular biology to the root hair phenotypes of multiple mutants and transgenic lines, including OX-ROP, CA-rop, aux1, axr3, tip1, eto1, etr1, and the triple mutant aux1 ein2 gnom eb.Conclusions/SignificanceWe show how interactions between Rho GTPases (in this case ROPs) and regulatory molecules (in this case auxin) could produce characteristic subcellular patterning that subsequently affects cell shape. This has important implications for research on the morphogenesis of plants and other eukaryotes. Our results also illustrate how gradient-regulated Turing systems provide a particularly robust and flexible mechanism for pattern formation.

Highlights

  • Rho small GTPases are a large family of highly conserved signalling proteins that contribute to biological processes as diverse as host-pathogen interactions, wound healing, development, and cancer [1,2]

  • In this model, unbinding of active Rho-of-Plants small GTPase (ROP) occurs at rate c, inactive ROP is created at rate b and active ROP at rate a

  • The mechanisms by which auxin influences ROP activity are not known, our results are strongly supportive of the hypothesis that a cellular auxin gradient upregulates the net amount of active ROP

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Summary

Introduction

Rho small GTPases are a large family of highly conserved signalling proteins that contribute to biological processes as diverse as host-pathogen interactions, wound healing, development, and cancer [1,2]. They play fundamental roles in eukaryotic cell division, cell morphogenesis and cell movement, through effects on actin and microtubule cytoskeletons, gene expression, and enzyme activity. The intracellular location of these proteins is important, and in plants the active forms of certain Rhos accumulate in patches that induce local cell outgrowths. Arabidopsis root hair cells produce patches of ROP at consistent and predictable subcellular locations, where root hair growth subsequently occurs

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