Open stomata 1 and phosphate starvation response 1 regulate tomato root system architecture during heterogeneous phosphate availability.

Plants frequently encounter uneven phosphate (Pi) distribution, yet most studies focuses on uniform low-Pi conditions. SUCROSE NONFERMENTING1-RELATED KINASE 2.6 (SnRK2.6) protein, also known as Open stomata 1 (OST1), is well-characterized in ABA signaling and stress responses. However, its role in low-Pi response is poorly understood. We investigated root system architecture (RSA) remodeling under uneven Pi distribution. Using split-root tomato plants with half roots in sufficient Pi (+Pi) and half in low Pi (-Pi), we observed low-Pi responses in both root sectors. Local low-Pi triggered the ABA accumulation in the local root regions, generating spatially distinct OST1 expression patterns. In mechanism, phosphate starvation response 1 (PHR1) directly binds to the OST1 promoter, activating its expression its expression under low-Pi conditions. This localized OST1 transcriptional regulation mediated both local and systemic RSA adaptations. Crucially, these Pi-responsive RSA remodeling were completely absent in ost1 and notabilis (not) mutants. These findings demonstrate that spatial phosphate availability shapes tomato root architecture through ABA-dependent OST1 activation and PHR1-mediated transcriptional regulation, identifying a previously unknown adaptive response to nutrient heterogeneity.