SlCAX3 drives the formation of crystal idioblasts for tomato ion compartmentalization under salt stress

Soil salinization severely limits global agricultural productivity. Although root ion exclusion and long-distance transport mechanisms are well studied, the spatial and cellular adaptations of photosynthetic leaf tissues to high-salinity microenvironments remain poorly understood. Here we generated a high-resolution spatiotemporal transcriptomic atlas of tomato leaves under long-term salt stress (LTSS) by integrating spatial transcriptomics (ST-seq) and single-nuclei RNA sequencing (snRNA-seq). Using pseudotime trajectory inference, multi-omics deconvolution, elemental analysis, and CRISPR-Cas9 genetic validation, we characterized cellular responses. LTSS induces heterogeneous transcriptional remodeling, reinforcing vascular structural stability while suppressing mesophyll photosynthesis. Notably, LTSS promotes explosive proliferation and developmental reprogramming of palisade mesophyll cells into specialized crystal idioblasts (CIs), driven by enhanced cell wall remodeling and microenvironmental crosstalk. Genetic studies confirm that the vacuolar transporter SlCAX3 is essential for CI formation. SlCAX3 has evolutionarily lost its conserved autoinhibitory N-terminal domain, potentially enabling high-flux ion transport. While SlCAX3-mediated CI formation does not reduce total foliar Na+ levels, it enables localized ion sequestration in CI vacuoles, thereby reducing oxidative damage and cytotoxicity in adjacent photosynthetic tissues. This work reveals spatially coordinated transcriptional responses and localized biomineralization as key strategies for tissue-level salt adaptation in tomato. The atypical structure of SlCAX3 supplements understanding of the conserved CAX1/3 transport system in land plants. These findings highlight localized cell-state transitions and ion sequestration as effective mechanisms to mitigate salt stress, providing genetic targets for breeding salt-tolerant crops.