Stress drives plasticity in leaf ageing transcriptional dynamics in Arabidopsis thaliana

Leaf development is dynamic, enabling plants to modulate their growth in response to environmental cues. Under drought conditions, for instance, the model plant Arabidopsis thaliana restricts leaf growth to conserve water, a strategy that enhances water-use efficiency. While this 'stress avoidance' response is well described physiologically, the underlying transcriptional changes that drive such developmental plasticity remain poorly understood. We investigated the transcriptional basis of how drought stress reshapes Arabidopsis leaf development. We profiled 1,226 leaves at various developmental stages and levels of drought stress, and generated a single-nucleus transcriptome atlas comprising ~1 million individual nuclei. We found that drought stress advances transcriptional programmes associated with leaf ageing in a dose-dependent manner, particularly within the mesophyll. These transcriptional shifts scale with stress intensity and correlate with reduced shoot growth, indicating that mesophyll-specific transcriptional changes underlie drought-induced restriction in leaf growth. Overexpression of FERRIC REDUCTION OXIDASE 6 (FRO6) in the mesophyll was sufficient to partially restore leaf growth under drought conditions. Our findings demonstrate how gene expression is reshaped by environmental cues to ensure that shoot architecture is adaptive to stress severity.