Drought tolerance is a pivotal trait for tomato (Solanum lycopersicum) genetic improvement, and enhancing the root/shoot ratio (R/S) serves as a core adaptive strategy for plants to cope with water deficit. While trehalose-6-phosphate phosphatase (TPP) genes are implicated in plant drought responses, their role in modulating R/S remains unclear. Here, we characterized SlTPP1 as a key positive regulator of drought tolerance in tomato. We found that drought stress dynamically induces SlTPP1 expression in roots while suppressing it in leaves. Mechanistically, SlTPP1 overexpression increases root soluble sugar content and upregulates night-specific expression of cell wall biosynthesis genes in roots to promote root growth, while concurrently suppressing the ethylene signaling pathway in leaves to increase R/S. Furthermore, we identified the transcription factor SlERF4 as a direct upstream repressor of SlTPP1. SlERF4 binds to the CE1 element (CACCG) in the SlTPP1 promoter and inhibits its transcription. CRISPR/Cas9-mediated knockout of SlERF4 results in enhanced drought tolerance, elevated SlTPP1 expression, increased R/S, and upregulation of root cell wall biosynthesis genes. Additionally, drought enhances ethylene biosynthesis in tomato leaves while concurrently reducing that in roots. Collectively, our study unveils a novel SlERF4–SlTPP1 regulatory module that enhances drought tolerance in tomato through the regulation of R/S, providing strategic targets for breeding drought-tolerant crops.

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