Natural variation links seedling hypocotyl growth with water loss in Arabidopsis

Plants integrate environmental and internal cues such as light and sugar availability to coordinate growth and water-use strategies. While hypocotyl elongation is widely used to study photo- and thermo-morphogenesis, its connection to whole-plant physiological traits remains unclear. Here, we uncover a negative correlation between hypocotyl length in young Arabidopsis thaliana seedlings and water loss in mature plants. Genome-wide association mapping across diverse natural accessions identified two genes, HEAT SHOCK TRANSCRIPTION FACTOR A2 (HSFA2) and a 2-oxoglutarate-dependent dioxygenase-like (2OGD-like), that affect hypocotyl elongation. Both genes are preferentially expressed in guard cells and are associated with reduced hypocotyl growth and increased stomatal conductance. Loss-of-function mutants displayed elongated hypocotyls and reduced gas exchange, whereas inducible and guard cell-specific expression of HSFA2 suppressed hypocotyl elongation and promoted stomatal opening. Guard cell transcriptomics and ChIP-seq analyses further revealed that HSFA2 directly targets genes involved in sugar signaling, light responses, and actin reorganization, including SCAR3, a component of the WAVE-ARP2/3 complex required for stomatal dynamics. Together, these findings establish a functional link between seedling growth and stomatal performance, expand the role of HSFA2 beyond heat responses, and position hypocotyl growth as a predictive platform for assessing plant water-use traits.