Spatial transcriptome analysis of the tea tender shoot sheds light on transcriptional regulation of characteristic metabolites

Abstract

The tender shoots of tea plant [Camellia sinensis (L.) Kuntze] contain characteristic flavor metabolites such as catechins, caffeine, and theanine, which are the raw materials for making various types of high-quality tea. The gene expression profiles with spatial information for tea shoots remain unclear, which has hindered the exploration of precise regulatory mechanisms of these characteristic metabolites in different cell types. Here, we provided a high-throughput analysis of the spatial gene expression of the tea shoot, including the apical bud, young leaf, and stem. The genome-wide expression pattern was delineated into nine representative spatial coexpression clusters, and cell type identification was achieved by integrating histological structures with marker gene annotation. The dynamic differentiation processes of cells in leaf and bud were revealed through the reconstruction of pseudotemporal trajectories, uncovering the coupling relationship between spatial organization and developmental progression. Gene Ontology enrichment analysis indicated that different clusters were enriched in functional pathways such as photosynthesis, cell wall construction, substance transport, and hormone response during differentiation, demonstrating their stage-specific expression throughout development. Additionally, we found that structural genes associated with the metabolism of catechins, theanine, and caffeine exhibited distinct spatial expression patterns across various tissues. Based on functional verification, we identified that the transcription factor gene CsTCP4 could positively regulate the biosynthesis of catechins and the hydrolysis of theanine. In conclusion, the spatial transcriptome atlas provides a foundational dataset for understanding gene expression heterogeneity in tea shoots and expands our understanding of the synergistic regulation of theanine and catechin metabolism in tea.

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (32502780), the Natural Science Foundation of Fujian Province (2025 J08070), the Young Backbone Faculty Fostering Fund of Anxi Tea College, Fujian Agriculture and Forestry University (ACKY2024002), and the Special Fund for Science and Technology Innovation of Fujian Zhang Tianfu Tea Development Foundation (FJZTF01). We thank Professor X. Xuhan of Fujian Agriculture and Forestry University for his help in the identification of tea cell types. We thank Biomarker Technologies Co., Ltd for assisting in sequencing of Spatial transcriptome.

Author contributions

C.Z. (Chengzhe Zhou) and Y.G. conceived and supervised this study; C.Z. (Cheng Zhang), C.T., S.W., A.Z., Z.R, and S.D. performed the experiments; C.Z. (Cheng Zhang), C.Z. (Chengzhe Zhou), S.S., Y.L., and C.T. analyzed the data; C.Z. (Cheng Zhang) and C.Z. (Chengzhe Zhou) wrote the paper; and C.Z. (Chengzhe Zhou) and Y.G. edited the paper.

Data availability

The raw sequencing data (spatial transcriptome) reported in this paper have been deposited in the National Genomics Data Center (https://ngdc.cncb.ac.cn/) under project number PRJCA025437.

Conflicts of interest statement

The authors declare no competing interests.

Supplementary material

Supplementary material is available at Horticulture Research online.

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