Extracellular matrix sensing by FERONIA and Leucine-Rich Repeat Extensins controls vacuolar expansion during cellular elongation in Arabidopsis thaliana.

Kai Dünser,Christoph Ringli,Jürgen Kleine‐Vehn,Mugurel I Feraru,Aline Herger,Shibu Gupta

doi:10.15252/embj.2018100353

Kai Dünser, Christoph Ringli + Show 4 more

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https://doi.org/10.15252/embj.2018100353

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Abstract

Cellular elongation requires the defined coordination of intra‐ and extracellular processes, but the underlying mechanisms are largely unknown. The vacuole is the biggest plant organelle, and its dimensions play a role in defining plant cell expansion rates. Here, we show that the increase in vacuolar occupancy enables cellular elongation with relatively little enlargement of the cytosol in Arabidopsis thaliana. We demonstrate that cell wall properties are sensed and impact on the intracellular expansion of the vacuole. Using vacuolar morphology as a quantitative read‐out for intracellular growth processes, we reveal that the underlying cell wall sensing mechanism requires interaction of extracellular leucine‐rich repeat extensins (LRXs) with the receptor‐like kinase FERONIA (FER). Our data suggest that LRXs link plasma membrane‐localised FER with the cell wall, allowing this module to jointly sense and convey extracellular signals to the cell. This mechanism coordinates the onset of cell wall acidification and loosening with the increase in vacuolar size.

Highlights

Primary plant cell walls are composed of the polysaccharides cellulose, hemicelluloses and pectin along with structural proteins
To assess the relative dilation of the vacuole, we combined the fluorescent dye BCECF (20,70-Bis-(2-carboxyethyl)-5-(and-6)-carboxyfluorescein), which accumulates in the vacuolar lumen of plant cells, with propidium iodide, which stains the exterior of the cells (Scheuring et al, 2015)
FER has been previously proposed to be required for cell wall sensing (Shih et al, 2014), but molecular interactors involved in the underlying mechanism were largely unknown

Summary

Introduction

Primary plant cell walls are composed of the polysaccharides cellulose, hemicelluloses and pectin along with structural proteins. The extracellular matrix features considerable tensile strength, withstanding the internal hydraulic turgor pressure of cells. This stiff construction provides stability to the plant body, yet obviously conflicts with cellular enlargements. Nuclear signalling of the phytohormone auxin is crucial for the control of extracellular pH and plant cell expansion in a concentration- and tissue-dependent manner (Spartz et al, 2014; Fendrych et al, 2016; Barbez et al, 2017). THESEUS1 (THE1) attenuates defects in cellulose deficiency, proposing a function of Catharanthus roseus receptor-like kinase 1-likes (CrRLK1Ls) in cell wall sensing (Hematy et al, 2007).

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