FERONIA and microtubules independently contribute to mechanical integrity in the Arabidopsis shoot.

Alice Malivert,Rodrigue Friaud,Özer Erguvan,Marjolaine Martin,Stéphane Verger,Antoine Chevallier,Mengying Liu,Théophile Peyraud,Olivier Hamant,Antoine Dehem,Mark Estelle

doi:10.1371/journal.pbio.3001454

Abstract

To survive, cells must constantly resist mechanical stress. In plants, this involves the reinforcement of cell walls, notably through microtubule-dependent cellulose deposition. How wall sensing might contribute to this response is unknown. Here, we tested whether the microtubule response to stress acts downstream of known wall sensors. Using a multistep screen with 11 mutant lines, we identify FERONIA (FER) as the primary candidate for the cell’s response to stress in the shoot. However, this does not imply that FER acts upstream of the microtubule response to stress. In fact, when performing mechanical perturbations, we instead show that the expected microtubule response to stress does not require FER. We reveal that the feronia phenotype can be partially rescued by reducing tensile stress levels. Conversely, in the absence of both microtubules and FER, cells appear to swell and burst. Altogether, this shows that the microtubule response to stress acts as an independent pathway to resist stress, in parallel to FER. We propose that both pathways are required to maintain the mechanical integrity of plant cells.

Highlights

All living organisms use mechanical forces as instructive cues during their development [1,2]
Plant cell walls are composed of load-bearing cellulose microfibrils, tethered by a matrix made of polysaccharides and structural proteins [6,7]
We focused on mutants impaired in receptor-like kinases that are highly expressed in the epidermis and aerial parts of the plant during early development and that exhibit an established link with the cell wall, namely feronia, theseus1, theseus1/ feronia-related1, curvy1, hercules receptor kinase 1, herk2, mdis1-interacting receptor-like kinase2, wall-associated kinase 1, wak2, wak3, and wak4

Summary

Introduction

All living organisms use mechanical forces as instructive cues during their development [1,2]. They share a common mechanical property: Cells are pressurized by osmotic pressure and experience cortical tension. Osmotic pressure in plants is several orders of magnitude higher than that of animal cells, and it is counterbalanced by stiff cell walls [3]. Regulating the mechanical properties of cell walls, through the perception of wall tension and integrity, is crucial for plant growth and development [4,5]. Plant cell walls are composed of load-bearing cellulose microfibrils, tethered by a matrix made of polysaccharides and structural proteins [6,7].

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Results

Conclusion