The mechanics of a stressful lifestyle: Deciphering the plant mechanostat

The physical mechanisms by which plant cells and tissues sense, process and respond to mechanical forces are poorly understood. Unraveling this is challenging as the mechanical signalling cascade involves a wide array of cellular structures and biomolecular effectors. Cells interact with their mechanical environment through their boundaries, the cell wall and plasma membrane. Forces are internalised through local structures, such as the cytoskeleton of protein filaments and transduced to the molecular scale, where force-induced conformational changes in mechanosensitive proteins convert mechanical cues into chemical signals and couple to the genetic machinery of the cell. Ultimately, mechanically-gated alterations of transcription patterns result in tensegrity adjustment, cell fortification and (re-)polarization. How this plant mechanostat realizes mechanical feedback at all these levels remains elusive, in particular as suitable model organisms that enable the quantitative study of mechanobiological feedback in a closed system and in a full three-dimensional context were absent to-date.

In this project, we will overcome these limitations by using the early Arabidopsis embryo as a comprehensive miniature model to explore how mechanical stimuli lead to cellular and genetic reprogramming. This project harnesses recent developments in the teams of the applicants to establish a toolkit of transgenic Arabidopsis lines marking crucial elements of the mechanostat (actin, tubulin, plasma membrane, tonoplast, SOSEKI polarity proteins), unique chemical mechanosensors and bespoke microfluidic devices for mechanical stimulation. In this project, this unique toolbox will be combined and put to work to explore mechanical feedback, quantitatively and in full three-dimensions, with unprecedented detail for the first time. We will describe the embryonic mechanostat, quantify the sensitivity and dose-response relationship of mechanical feedback to a wide variety of mechanotranductory components in the cell, unveil the role of mechanical signalling in biological function and development and establish how mechanical cues instruct the genetic reprogramming of plant cells.