Water fluxes pattern growth and identity in shoot meristems

• Published in: Nature communications 2024-08, Vol.15 (1), p.6944-14, Article 6944
• Main Authors: Alonso-Serra, Juan, Cheddadi, Ibrahim, Kiss, Annamaria, Cerutti, Guillaume, Lang, Marianne, Dieudonné, Sana, Lionnet, Claire, Godin, Christophe, Hamant, Olivier
• Format: Article
• Language: English
• Subjects: 14; 14/19; 14/34; 14/63; 38; 38/91; 45; 631/449/2653/1359; 631/449/2653/2655; 631/57/2266; 64; Arabidopsis - growth & development; Arabidopsis - metabolism; Atrophy; Biological Physics; Botanics; Development Biology; Fluid flow; Fluxes; Growth conditions; Humanities and Social Sciences; Hydraulics; Life Sciences; Meristem - growth & development; Meristem - metabolism; Meristems; Morphogenesis; multidisciplinary; Organs; Physics; Plant cells; Plant Shoots - growth & development; Plant Shoots - metabolism; Science; Science (multidisciplinary); Shoots; Vegetal Biology; Volumetric analysis; Water - metabolism; Water deficit; Water flow
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-51099-x

In multicellular organisms, tissue outgrowth creates a new water sink, modifying local hydraulic patterns. Although water fluxes are often considered passive by-products of development, their contribution to morphogenesis remains largely unexplored. Here, we mapped cell volumetric growth across the shoot apex in Arabidopsis thaliana . We found that, as organs grow, a subpopulation of cells at the organ-meristem boundary shrinks. Growth simulations using a model that integrates hydraulics and mechanics revealed water fluxes and predicted a water deficit for boundary cells. In planta , a water-soluble dye preferentially allocated to fast-growing tissues and failed to enter the boundary domain. Cell shrinkage next to fast-growing domains was also robust to different growth conditions and different topographies. Finally, a molecular signature of water deficit at the boundary confirmed our conclusion. Taken together, we propose that the differential sink strength of emerging organs prescribes the hydraulic patterns that define boundary domains at the shoot apex. Combining cell volumetric analysis, growth simulation, and in planta water flow tracing, the authors reveal the correlation between water flux distribution and cell growth rate in Arabidopsis shoot apex, suggesting the potential contribution of hydraulic patterns to morphogenesis.