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

ABSTRACT: Soil salinization is a primary constraint on global agricultural productivity. While the mechanisms of root ion exclusion and whole-plant long-distance transport are well established, how photosynthetic leaf tissues complexly adapt to high-salinity microenvironments at the spatial and cellular level remains a critical blind spot in plant stress biology. We integrated spatial transcriptomics (ST-seq) and single-nuclei RNA sequencing (snRNA-seq) to construct a high-resolution spatiotemporal transcriptomic atlas of tomato leaves subjected to long-term salt stress (LTSS). We combined pseudotime trajectory inference, multi-omics deconvolution, elemental analysis, and CRISPR-Cas9-mediated genetic validation to elucidate cellular responses. LTSS induces heterogeneous transcriptional remodeling across leaf tissues, primarily reinforcing vascular structural stability while suppressing mesophyll photosynthesis. Concurrently, LTSS triggers the explosive proliferation and developmental reprogramming of palisade mesophyll cells into highly specialized crystal idioblasts (CIs). This cell fate transition is orchestrated by enhanced cell wall remodeling and intensive microenvironmental crosstalk. Genetic analyses establish that the vacuolar transporter SlCAX3 is essential for CI formation. Sequence and structural evaluations indicate that SlCAX3 evolutionarily lost its conserved autoinhibitory N-terminal domain, a structural specialization that may support high-flux ion transport. Although SlCAX3-driven CI formation does not reduce total foliar Na⁺ content, it facilitates localized ion sequestration within CI vacuoles, which is associated with mitigated oxidative damage and cytotoxicity in adjacent photosynthetic tissues. This study demonstrates that tissue-level salt adaptation in tomato involves spatially coordinated transcriptional responses and localized biomineralization. The identification of SlCAX3's atypical architecture provides a functional supplement to the conserved CAX1/3 transport system in land plants. Our findings highlight localized cell-state transitions and ion sequestration as an effective tissue-level strategy for mitigating salt stress, offering strategic genetic targets for breeding climate-resilient crops.

ORGANISM(S): Solanum lycopersicum

PROVIDER: GSE325371 | GEO | 2026/03/20

REPOSITORIES: GEO

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Project description:Purpose: Grafting is a commonly used cultural practice to counteract salt stress and is especially important for vegetable production. However, it is not clear which metabolic processes and genes are involved in the response of tomato rootstocks to salt stress. Our goals is to elucidate the regulatory mechanism through which grafting enhances salt tolerance. Methods: The salt-sensitive tomato variety Zhongza 9 and the strongly salt-tolerant tomato rootstock variety QZ-006 (selected by the research group in the early stage) were used as experimental materials and were purchased from the Vegetable and Flower Institute of the Chinese Academy of Agricultural Sciences (Beijing, CHN) and Beijing Kaixingelin Agricultural Technology Co., Ltd. (Beijing, CHN)；The leaves of the seedlings of every sample was added to 5 mL of HNO3 (65%~68%) after they were heated in a microwave digestion system for 2~3 hours；RNA-seq libraries were sequenced on an Illumina HiSeq X Ten platform；qRT‒PCR was performed according to the instructions of a Fast Super EvaGreen qPCR Master Mix Kit (US Everbright®, Inc.)；The amino acid contents in the tomato leaves were calculated by the external standard method. The chlorophyll of the seedlings was extracted with acetone-ethanol (1:1) ；An indirect enzyme-linked immunosorbent assay (ELISA) was used to determine auxin (IAA), gibberellin (GA), cytokinin (ZR), brassinolide (BR), abscisic acid (ABA), jasmonic acid (JA) and salicylic acid (SA) contents, and kit purchased from ThermoFisher Scientific Co., Ltd. (USA). Endogenous ethylene (ETH) was collected, fixed and determined according to the methods of Ling (Ling et al.,2008) using a Shimadzu 2010 gas chromatograph equipped with a hydrogen flame ion detector. ETH standard gas was purchased from Sigma Company. Results: Compared with the NGS, the GSs were more salt tolerant, and the Na+ content in the leaves decreased significantly. Through transcriptome sequencing data analysis of 36 samples, we found that GSs exhibited more stable gene expression patterns, with a lower number of DEGs. WRKY and PosF21 transcription factors were significantly upregulated in the GSs compared to the NGSs. Moreover, the GSs presented more amino acids, a higher photosynthetic index and a higher content of growth-promoting hormones. The main differences between GSs and NGSs were in the expression levels of genes involved in the BR signalling pathway, with significant upregulation of XTHs. Conclusions: Our study demonstrates that grafting on salt tolerant rootstocks can bring different metabolic processes and transcription levels changes to scion leaves, thereby the scion leaves show stronger salt tolerance. This information provides new insight into the mechanism underlying tolerance to salt stress regulation and provides useful molecular biological basis for improving plant salt resistance.

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

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