The role of mechanical signals in cell identity determination remains poorly explored in tissues. Furthermore, because mechanical stress is widespread, mechanical signals are difficult to uncouple from biochemical-based transduction pathways. Here we focus on the homeobox gene SHOOT MERISTEMLESS (STM), a master regulator and marker of meristematic identity in Arabidopsis. We found that STM expression is quantitatively correlated to curvature in the saddle-shaped boundary domain of the shoot apical meristem. As tissue folding reflects the presence of mechanical stress, we test and demonstrate that STM expression is induced after micromechanical perturbations. We also show that STM expression in the boundary domain is required for organ separation. While STM expression correlates with auxin depletion in this domain, auxin distribution and STM expression can also be uncoupled. STM expression and boundary identity are thus strengthened through a synergy between auxin depletion and an auxin-independent mechanotransduction pathway at the shoot apical meristem.
The bending, stretching or squashing of cells or tissues can be used as a signal to trigger a range of biological responses. However investigating the role of these mechanical signals remains a challenge. This is partly because the forces that trigger the mechanical signals are often short-lived and changeable, and partly because the signals can be difficult to separate from the biochemical responses that they generate.
Stem cells present at the tip of the growing shoots in a plant are exposed to mechanical forces. These growing tips are called shoot meristems, and the stem cells they contain create all the aboveground organs of the plant (stems, leaves and flowers etc.). In each meristem, a boundary forms between the slow-growing stem cells at its centre and the fast-growing organs that form around them. Because these plant cells are both stuck together by their cell walls and growing at different rates, strong mechanical stresses are created causing this boundary to fold. A key regulator of the meristem is a protein called STM, but it remains unclear whether mechanical signals are involved in the control of this protein.
To investigate this, Landrein et al. tracked where the gene for the STM protein was switch on in shoot meristems in a plant called Arabidopsis, and found that it is highly active at the boundary. Analysing STM in different mutant plants combined with advanced imaging techniques revealed that STM activity correlates with the extent of creasing at this boundary. The STM protein is also required at the boundary to ensure that developing organs separate out. These findings suggest that boundary folding might somehow create signals that activate STM. One candidate signal was the plant hormone called auxin because reduced levels of this hormone were previously associated with boundary formation. However, in further experiments, Landrein et al. ruled out auxin’s involvement in this process.
So do mechanical signals activate STM at the boundary? To test this, the mechanical forces in the meristem were altered by compressing the growing shoot meristems in miniature vices and by killing a few stem cells at the meristem centre. Both of these actions triggered the production of STM in the meristem, consistent with its activity being altered by mechanical stress.
Landrein et al. propose that the mechanical regulation identified acts in parallel to auxin signalling, providing robustness to the regulation of gene activity in the shoot meristem. In other words, tissue folding can guide gene expression, via the production of mechanical signals. But how shoot meristem cells respond at a molecular level to mechanical stress awaits future work. Finally, proteins related to STM can be found in all biological kingdoms, including some proteins that regulate important process in animal development. Whether the activity of these related proteins is also regulated by mechanical forces remains to be investigated.