The air is dry: a quest to safeguard plants from a hotter and drier future (DRY-AIR)

Global climate change is intensifying drought events, threatening plant survival, agricultural productivity, and ecosystem stability. While drought is traditionally associated with soil water deficits, recent evidence highlights the critical role of atmospheric drought, quantified as Vapor Pressure Deficit (VPD), in shaping plant responses to water stress. Elevated VPD increases atmospheric evaporative demand, enhancing transpiration rates and imposing significant challenges to plant water balance. Despite its growing relevance, the physiological and molecular mechanisms underlying plant adaptation to high VPD remain poorly understood. In this study, we investigated the early responses of Arabidopsis thaliana seedlings to elevated VPD, isolating atmospheric drought from soil water limitations using a hydroponic system. This approach enabled us to assess shoot-specific responses while maintaining stable root hydration, ensuring that observed effects were driven solely by changes in air humidity. Our results reveal that high VPD triggers an immediate and dynamic stomatal response, leading to a rapid reduction in stomatal aperture and increased leaf temperature due to reduced transpirational cooling. At the molecular level, transcriptomic analysis unveiled a rapid and sustained activation of stress-responsive genes in the shoot, particularly those involved in abscisic acid (ABA) biosynthesis and signalling. The strong upregulation of ABA-related genes supports its central role in mediating stomatal responses to VPD stress. In contrast, auxin-related genes were significantly downregulated, suggesting a trade-off between stress adaptation and growth regulation. Notably, while shoot responses were immediate, root responses were delayed, indicating the activation of a systemic shoot-to-root signalling pathway. This highlights the role of the shoot as the primary sensor of atmospheric drought, transmitting signals to the root system to coordinate whole-plant acclimation. These findings provide novel insights into the molecular and physiological mechanisms by which plants perceive and respond to atmospheric drought. By elucidating the early signalling events and regulatory networks involved in VPD-induced stress, this study contributes to a deeper understanding of plant water-use efficiency and drought resilience. In a context of increasing climate variability and water scarcity, these insights pave the way for future strategies aimed at improving crop adaptation to environmental stress, ensuring agricultural sustainability in a rapidly changing world.