Water fluxes contribute to growth patterning in shoot meristems

In multicellular organisms, localized tissue outgrowth creates a new water sink thereby modifying hydraulic patterns at the organ level. These fluxes are often considered passive by-products of development and their patterning and potential contribution to morphogenesis remains largely unexplored. Here, we generated a complete map of cell volumetric growth and deformation across the shoot apex in Arabidopsis thaliana. Within the organ-meristem boundary, we found that a subpopulation of cells next to fast-growing cells experiences volumetric shrinkage. To understand this process, we used a vertex-based model integrating mechanics and hydraulics, informed by the measured growth rates. Organ outgrowth simulations revealed the emerging water fluxes and predicted water deficit with volume loss for a few cells at the boundary. Consistently, in planta, a water-soluble dye is preferentially allocated to fast-growing tissues and fails to enter the boundary domain. Analysis of intact meristems further validated our model by revealing cell shrinkage next to fast-growing cells in different contexts of tissue surface curvature and cell deformation. A molecular signature of water deficit at the boundary further confirmed our conclusion. Taken together, we propose a model where the differential sink strength of emerging organs prescribes the hydraulic patterns that define the boundary domain at the shoot apex.