Epidermal hydrodynamics controls water homeostasis of shoot meristems for plant adaptation to terrestrial environments

Water uptake and redistribution represent a significant challenge for plant colonization of land. While vascular plants have evolved specialized structures for water transport, how water homeostasis is maintained in meristematic tissues remains elusive. Here, we show that the Arabidopsis shoot meristem develops within a high-humidity niche. The homeodomain leucine zipper (HD-ZIP) transcription factor ARABIDOPSIS THALIANA MERISTEM LAYER 1 (ATML1) and its regulatory target PIP2;5 establish a water conduit across L1 cells to facilitate hydraulic exchange with the surrounding microenvironment. The ATML1-PIP2;5 module regulates stem cell activity in response to humidity fluctuations and is associated with local adaptation to arid climates in natural populations. Transcriptional activation of water flux by class IV homeodomain-leucine zipper (C4HDZ) proteins predates the emergence of vascular systems, contributing to hydraulic response in the liverwort Marchantia polymorpha. Our results reveal an evolutionarily conserved epidermal hydraulic pathway that integrates developmental patterning with environmental sensing, highlighting a fundamental role for the shoot meristem in shaping plant adaptation in terrestrial habitats.