The Specification of Geometric Edges by a Plant Rab GTPase Is an Essential Cell-Patterning Principle During Organogenesis in Arabidopsis

Charlotte Kirchhelle,Cheung-Ming Chow,Camille Foucart,Helia Neto,York-Dieter Stierhof,Monika Kalde,Carol Walton,Mark Fricker,Richard S Smith,Antoine Jérusalem,Niloufer Irani,Ian Moore

doi:10.1016/j.devcel.2016.01.020

Abstract

SummaryPlant organogenesis requires control over division planes and anisotropic cell wall growth, which each require spatial patterning of cells. Polyhedral plant cells can display complex patterning in which individual faces are established as biochemically distinct domains by endomembrane trafficking. We now show that, during organogenesis, the Arabidopsis endomembrane system specifies an important additional cellular spatial domain: the geometric edges. Previously unidentified membrane vesicles lying immediately beneath the plasma membrane at cell edges were revealed through localization of RAB-A5c, a plant GTPase of the Rab family of membrane-trafficking regulators. Specific inhibition of RAB-A5c activity grossly perturbed cell geometry in developing lateral organs by interfering independently with growth anisotropy and cytokinesis without disrupting default membrane trafficking. The initial loss of normal cell geometry can be explained by a failure to maintain wall stiffness specifically at geometric edges. RAB-A5c thus meets a requirement to specify this cellular spatial domain during organogenesis.

Highlights

A central question in morphogenesis is how the behavior of individual cells is coordinated to generate the stereotypical multiscale organization of cells, tissues, and organs during embryogenesis (Blanchard and Adams, 2011)
Polyhedral plant cells can display complex patterning in which individual faces are established as biochemically distinct domains by endomembrane trafficking
We show that, during organogenesis, the Arabidopsis endomembrane system specifies an important additional cellular spatial domain: the geometric edges

Summary

Introduction

A central question in morphogenesis is how the behavior of individual cells is coordinated to generate the stereotypical multiscale organization of cells, tissues, and organs during embryogenesis (Blanchard and Adams, 2011). Cell geometry in turn influences the capacity of cells to respond to chemical and mechanical signals (Bassel et al, 2014; Sampathkumar et al, 2014) that act on fields of cells to coordinate their individual polarization with respect to microtubule organization, auxin transport, and wall extensibility (Heisler et al, 2010; Nakayama et al, 2012; Peaucelle et al, 2011, 2015; Ray et al, 2015; Robinson et al, 2013) All these features of regulative development require spatial patterning of cells

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Discussion

Conclusion