Mass spectrometry imaging and single-cell transcriptional profiling reveal the tissue-specific regulation of bioactive ingredient biosynthesis in Taxus leaves

Zhan, Xiaowei; Qiu, Tian; Zhang, Hongshan; Hou, Kailin; Liang, Xueshuang; Chen, Cheng; Wang, Zhijing; Wu, Qicong; Wang, Xiao-Jia; Li, Xin; Wang, Mingshuang; Feng, Shi Ting; Zeng, Houqing; Yu, Chunna; Wang, Huizhong; Shen, Chenjia

doi:10.1016/j.xplc.2023.100630

Cited by 19 publications

(12 citation statements)

References 62 publications

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“…However, we analyzed the expression patterns of the characterized genes involved in the gypenosides biosynthesis pathway at single-cell resolution to explore the spatial distribution of this pathway in G. pentaphyllum shoot apexes and leaves revealed that gypenoside biosynthesis is predominantly localized in MCs. Similarly, taxol biosynthesis was observed in MCs of Taxus leaves, as evidenced by the scRNA-seq data analysis ( Zhan et al., 2023 ). These findings suggest that the biosynthesis of both gypenoside and taxol does not involve multicellular compartmentalization.…”

Section: Discussionmentioning

confidence: 75%

“…The integration of scRNA-seq with mass spectrometry imaging technology can further enhance our ability to explore the spatial organization of specialized metabolism. A combination of two technologies revealed that the majority of taxol biosynthesis genes are predominantly expressed in leaf mesophyll cells (MCs), while phenolic acid and flavonoid biosynthesis genes are highly expressed in leaf ECs ( Zhan et al., 2023 ). In addition, a single-cell transcriptome atlas of tea leaves was constructed and a novel catechin ester glycosyltransferase was characterized by a gene coexpression network in MCs, suggesting that scRNA-seq has great potential for the screening and identifying genes involved in the biosynthesis of plant specialized metabolites ( Wang et al., 2022 ).…”

Section: Introductionmentioning

confidence: 99%

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Single-cell transcriptome profiling reveals the spatiotemporal distribution of triterpenoid saponin biosynthesis and transposable element activity in Gynostemma pentaphyllum shoot apexes and leaves

Li,

Du,

Zhang

et al. 2024

Front. Plant Sci.

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Gynostemma pentaphyllum (Thunb.) Makino is an important producer of dammarene-type triterpenoid saponins. These saponins (gypenosides) exhibit diverse pharmacological benefits such as anticancer, antidiabetic, and immunomodulatory effects, and have major potential in the pharmaceutical and health care industries. Here, we employed single-cell RNA sequencing (scRNA-seq) to profile the transcriptomes of more than 50,000 cells derived from G. pentaphyllum shoot apexes and leaves. Following cell clustering and annotation, we identified five major cell types in shoot apexes and four in leaves. Each cell type displayed substantial transcriptomic heterogeneity both within and between tissues. Examining gene expression patterns across various cell types revealed that gypenoside biosynthesis predominantly occurred in mesophyll cells, with heightened activity observed in shoot apexes compared to leaves. Furthermore, we explored the impact of transposable elements (TEs) on G. pentaphyllum transcriptomic landscapes. Our findings the highlighted the unbalanced expression of certain TE families across different cell types in shoot apexes and leaves, marking the first investigation of TE expression at the single-cell level in plants. Additionally, we observed dynamic expression of genes involved in gypenoside biosynthesis and specific TE families during epidermal and vascular cell development. The involvement of TE expression in regulating cell differentiation and gypenoside biosynthesis warrant further exploration. Overall, this study not only provides new insights into the spatiotemporal organization of gypenoside biosynthesis and TE activity in G. pentaphyllum shoot apexes and leaves but also offers valuable cellular and genetic resources for a deeper understanding of developmental and physiological processes at single-cell resolution in this species.

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Section: Discussionmentioning

confidence: 75%

Section: Introductionmentioning

confidence: 99%

Single-cell transcriptome profiling reveals the spatiotemporal distribution of triterpenoid saponin biosynthesis and transposable element activity in Gynostemma pentaphyllum shoot apexes and leaves

Li,

Du,

Zhang

et al. 2024

Front. Plant Sci.

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“…Bark contains a large number of active ingredients, but it is a nonrenewable resource. Due to its sufficient biomass and renewable characteristics, the Taxus leaf is a primary resource used for industrial extraction . In the past few years, a number of active ingredients have been detected and isolated from the leaves of different Taxus species .…”

Section: Introductionmentioning

confidence: 99%

“…cuspidata . Due to the tissue specificity of gene expression, understanding the location of metabolites can be helpful in deciphering their biosynthetic pathways. , Data on the spatial distribution of active ingredients can also provide guidance for sampling for the pharmaceutical industry. However, the precise spatial distribution of active ingredients in the leaves of T.…”

Section: Introductionmentioning

confidence: 99%

“…Due to its sufficient biomass and renewable characteristics, the Taxus leaf is a primary resource used for industrial extraction. 13 In the past few years, a number of active ingredients have been detected and isolated from the leaves of different Taxus species. 14 In plants, the leaf is the primary organ for photosynthesis and carbon fixation, harboring various types of tissues.…”

Section: Introductionmentioning

confidence: 99%

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Mass Spectrometry-Imaging Analysis of Active Ingredients in the Leaves of Taxus cuspidata

Zhan,

Zang,

et al. 2024

ACS Omega

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Background: Taxus cuspidata is an endangered evergreen conifer mainly found in Northeast Asia. In addition to the well-known taxanes, several active ingredients were detected in the leaves of T. cuspidata. However, the precise spatial distribution of active ingredients in the leaves of T. cuspidata is largely unknown. Results: in the present study, timsTOF flex MALDI-2 analysis was used to uncover the accumulation pattern of active ingredients in T. cuspidata leaves. In total, 3084 ion features were obtained, of which 944 were annotated according to the mass spectrometry database. The principal component analysis separated all of the detected metabolites into four typical leaf tissues: mesophyll cells, upper epidermis, lower epidermis, and vascular bundle cells. Imaging analysis identified several leaf tissues that specifically accumulated active ingredients, providing theoretical support for studying the regulation mechanism of compound biosynthesis. Furthermore, the relative accumulation levels of each identified compound were analyzed. Two flavonoid compounds, ligustroflavone and Morin, were identified with high content through quantitative analysis of the ion intensity. Conclusions: our data provides fundamental information for the protective utilization of T. cuspidata.

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Single-cell transcriptional profiling reveals cell type-specific responses to duck reovirus infection in the Bursa of Fabricius of Cairna moschata

Yun,

Hua,

et al. 2024

International Journal of Biological Macromolecules

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Mass spectrometry imaging and single-cell transcriptional profiling reveal the tissue-specific regulation of bioactive ingredient biosynthesis in Taxus leaves

Cited by 19 publications

References 62 publications

Single-cell transcriptome profiling reveals the spatiotemporal distribution of triterpenoid saponin biosynthesis and transposable element activity in Gynostemma pentaphyllum shoot apexes and leaves

Single-cell transcriptome profiling reveals the spatiotemporal distribution of triterpenoid saponin biosynthesis and transposable element activity in Gynostemma pentaphyllum shoot apexes and leaves

Mass Spectrometry-Imaging Analysis of Active Ingredients in the Leaves of Taxus cuspidata

Single-cell transcriptional profiling reveals cell type-specific responses to duck reovirus infection in the Bursa of Fabricius of Cairna moschata

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