Single‐cell transcriptome atlas reveals developmental trajectories and a novel metabolic pathway of catechin esters in tea leaves

Abstract

The tea plant is an economically important woody beverage crop. The unique taste of tea is evoked by certain metabolites, especially catechin esters, whereas their precise formation mechanism in different cell types remains unclear. Here, a fast protoplast isolation method was established and the transcriptional profiles of 16 977 single cells from 1st and 3rd leaves were investigated. We first identified 79 marker genes based on six isolated tissues and constructed a transcriptome atlas, mapped developmental trajectories and further delineated the distribution of different cell types during leaf differentiation and genes associated with cell fate transformation. Interestingly, eight differently expressed genes were found to co-exist at four branch points. Genes involved in the biosynthesis of certain metabolites showed cell-and development-specific characteristics. An unexpected catechin ester glycosyltransferase was characterized for the first time in plants by a gene co-expression network in mesophyll cells. Thus, the first single-cell transcriptional landscape in woody crop leave was reported and a novel metabolism pathway of catechin esters in plants was discovered.

Integrated mass spectrometry imaging and single‐cell transcriptome atlas strategies provide novel insights into taxoid biosynthesis and transport in Taxus mairei stems

“…Recent T. mairei genome information and optimized protoplast isolation protocols have facilitated the generation of a comprehensive single-cell transcriptional Taxus stem landscape (Xiong et al, 2021). Our scRNA-seq analysis produced a pool of 21 233 cells (average 7078 cells in each repeat), which was larger than that of poplar scRNA-seq (3626 and 3170 cells from bark and wood tissue, respectively) and similar to that of tea tree scRNA-seq (9458 and 7519 cells from first and third leaves, respectively), but lower than that of rice (Oryza sativa) (237 431 cells from leaves and roots) and Arabidopsis (36 643 cells from the vegetative shoot apex) (Chen, Tong, et al, 2021;Wang et al, 2022;Wang, Huan, et al, 2021;Zhang et al, 2021). Sufficient cells ensured that our genome-scale expression profiling covered all stem cell types.…”

“…Cell annotations are required to define cell types in non‐model plants. Some marker genes in model plants, e.g., Arabidopsis, express homologous genes which show similar expression patterns when compared with woody trees (Chen, Tong, et al., 2021; Wang et al., 2022). In our study, 13 cluster‐specific markers were used to annotate cell types in T. mairei stems.…”

“…The technology was instrumental in identifying several organ development‐related regulators, including epidermis development regulators, TFs regulating mesophyll cell development, regulators involved in the developmental trajectories of floret and inflorescence meristems, regulators of wood formation processes in poplar, and novel regulators required for the early development of vein patterns in cotyledons (Chen, Tong, et al., 2021; Liu, Guo, et al., 2022; Liu, Wang, et al., 2022; Tao et al., 2022; Zong et al., 2022). Similarly, single‐cell transcriptome atlases have been used to identify novel catechin ester metabolic pathways in tea trees and provided novel scRNA‐seq applications to study plant secondary metabolism (Wang et al., 2022).…”

Single‐cell transcriptomic analyses reveal cellular and molecular patterns of rubber tree response to early powdery mildew infection

“…With this technology, it is possible to explore the heterogeneity among different cell types in complex tissues and to identify unknown cell types. Many single‐cell transcriptomic atlases have been established successfully for various crops, including rice, maize, peanuts and tea (Liu et al, 2021; Wang et al, 2021; Wang et al, 2022; Xu et al, 2021). These atlases lay the foundation for the functional characterization and manipulation of candidate genes that are needed to develop elite cultivars.…”

Single‐cell RNA‐seq reveals fate determination control of an individual fibre cell initiation in cotton (Gossypium hirsutum)

“…Subsequently, a series of developmental processes in Arabidopsis had been explored at single cell resolution, such as the development of root tips (Denyer et al ., 2019 ; Jean‐Baptiste et al ., 2019 ; Shahan et al ., 2022 ; Wendrich et al ., 2020 ; Zhang et al ., 2019 ), lateral root (Gala et al ., 2021 ), vegetative shoot apex (Zhang et al ., 2021b ), stomatal cell lineage (Liu et al ., 2020 ), developing leaf (Kim et al ., 2021 ; Liu et al ., 2022a ; Lopez‐Anido et al ., 2021 ; Tenorio Berrio et al ., 2022 ) and vein pattern in the cotyledons (Liu et al ., 2022b ). At the same time, scRNA‐seq has also been widely used in other plants, including rice (Liu et al ., 2021b ; Wang et al ., 2021b ; Zhang et al ., 2021a ; Zong et al ., 2022 ), corn (Li et al ., 2022 ; Ortiz‐Ramirez et al ., 2021 ; Satterlee et al ., 2020 ; Sun et al ., 2022 ; Xu et al ., 2021 ), peanut (Liu et al ., 2021a ), tea plant (Wang et al ., 2022 ), tomato (Omary et al ., 2022 ) and poplar (Chen et al ., 2021 ; Li et al ., 2021 ; Xie et al ., 2022 ). These studies provide new insights into heterogeneity of gene expression between different cell types, and molecular trajectory of cell differentiation during development.…”