A SlERF4–SlTPP1 module enhances drought tolerance in tomato by increasing the root/shoot ratio

Abstract

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.

Acknowledgements

We would like to thank Prof. Xia Cui from the Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, for providing the overexpression and knockout vectors and for providing assistance in tomato genetic transformation. This research was supported by the National Key Research and Development Program of China (2023YFD2300700, 2021YFD1600300, and 2024YFD2300702), China Agriculture Research System (CARS-23-B07), and the National Natural Science Foundation of China (Grant No. 32502804).

Author contributions

H.W., W.J., X.Y., and Q.L. conceived the experiments. H.W., L.C., and H.Y. performed the experiments. H.W. and L.C. wrote the paper. H.L., D.Y., S.I., T.L., and Y.L. revised the manuscript. All authors discussed and approved the final manuscript.

Data availability

RNA sequencing data were deposited to SRA (https://www.ncbi.nlm.nih.gov/sra) with BioProject accession number PRJNA1366651 (root) and PRJNA1367885 (leaf). The data underlying this article are available in the article and in its online supplementary material.

Conflicts of interest statement

The authors declare no conflicts of interest.

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