Research Group Stanislas
Plasma Membrane and Mechano-Perception in Plant Development
Mechanical signals and morphogenesis at the plant shoot stem cell niche
Morphogenesis, both at the cell and tissue level, involves mechanical signals that influence specific patterns of gene expression and trigger cytoskeletal reorganisations. How a mechanical stress is perceived and how this signal is transduced into the cell to exert these effects is still poorly understood, and remains a challenging question in both the plant and animal community.
In plants, the emergence of all aerial organs occurs post-embryogenesis from an organized stem cell niche called the shoot apical meristem (SAM). From the 1980s onwards, research into the genetic basis of meristem function identified key regulators of stem cell homeostasis and organogenesis. In the 2000s, these molecular analyses were extended by addressing the dynamic behaviours of hormones at the SAM. More recently, the structural elements of meristematic cells have become the focus of attention.
Plant cells grow through increase in volume and cell wall surface area, which is driven by an internal hydrostatic pressure, the turgor pressure, and is constrained by the resistance of the cell walls that surround almost all cells. Cortical microtubules (MTs) orient parallel to the maximal tensile stress direction (4). Since deposition of newly synthesized cell wall components (cellulose mirofibrils) are guided by cortical MTs, the stress pattern will modify cell wall mechanical anisotropy and the growth direction, giving rise to a new shape and a new mechanical stress pattern, creating a mechanical feedback loop. Mutants that perturb this feedback loop, such as katanin which perturbs microtubule severing, display a severely dwarfed phenotype with smaller leaves and floral organs, and fruits that are short and thick, illustrating the importance of mechanical signalling for normal SAM function and organogenesis. Among the structural components of plant cells, the plasma membrane (PM) has received very little attention. Yet its position at the interface between the cell wall and the cytoplasmic microtubule arrays makes it a key factor at the nexus between biochemical and mechanical cues.
Whereas phosphatidylinositol phosphates (PIPs) have been involved in almost all biological functions, including stem cell maintenance and organogenesis in animals, the processes in meristem biology to which PIPs contribute still need to be delineated. Using specific PIPs biosensors for PI4P and PI(4,5)P2, the two most abundant PIPs at the plasma membrane, we reveal that meristem functions are associated with a stereotypical PIP tissue-scale pattern. Interestingly, this pattern echoes that of cortical microtubules and stress anisotropy at the meristem. While other cues are very likely to contribute to the final PIP pattern, we provide evidence that the patterns of PIP, cortical microtubules and mechanical stress are positively correlated, suggesting that the PIP pattern, and its reproducibility, relies at least in part on the mechanical status of the SAM.
Given these observations, we are now in a unique position to address the following questions:
- What is the contribution of the PIP pattern to SAM function?
- What are the functions of PIPs in mechanotransduction?
- What is the molecular relation between the PM and mechano-responsive elements?