Zhang Bingxu, Lam Thomas Ka Yam, Chen Linheng, Zhang Chen, Zhu Liping, Zhang Hailei, Wang Pengxi, Wang Jianing, Cai Zongwei, Xia Yiji
Department of Biology, Hong Kong Baptist University, Hong Kong SAR, China.
Department of Chemistry, Hong Kong Baptist University, Hong Kong SAR, China.
BMC Biol. 2025 Jul 1;23(1):191. doi: 10.1186/s12915-025-02297-6.
Understanding the spatiotemporal regulation of specialized metabolism in plants is critical for advancing both basic plant biology and biotechnological applications. PRODUCTION OF ANTHOCYANIN PIGMENT 1 (PAP1) is a well-known transcription factor that plays a key regulatory role in the biosynthesis pathway of plant flavonoids. Similar to other secondary metabolites, flavonoid biosynthesis displays cell heterogeneity. However, the cell-specific regulation network of the flavonoid biosynthetic pathway remains unclear.
In this study, we utilized single-cell RNA sequencing (scRNA-seq) and time-series metabolite profiling to investigate the regulation of flavonoid biosynthesis and phytohormone homeostasis in Arabidopsis thaliana by PAP1. By comparing single-cell transcriptomes of the pap1-D mutant and wild-type plant leaves, we constructed a cell-type-specific atlas of gene expression and high-resolution dynamics of metabolites across developmental stages. Our findings reveal that PAP1 overexpression induces distinct spatiotemporal regulation of phenylpropanoid pathway genes in different cell types and widespread upregulation of glycosylation processes. Metabolomic profiling validated these transcriptional patterns and showed significant changes of metabolites in phenylalanine metabolic processes as pap1-D leaf matures. Additionally, PAP1 overexpression leads to significant changes in phytohormone levels, particularly jasmonate and salicylate, indicating complex crosstalk between flavonoid biosynthesis and hormone homeostasis.
This integrated multi-omics approach provides unprecedented insights into the cell-specific regulatory networks controlling specialized metabolism and establishes a valuable framework for optimizing metabolic engineering strategies to enhance the production of bioactive plant compounds.
了解植物中特殊代谢的时空调控对于推进基础植物生物学和生物技术应用都至关重要。花青素色素合成蛋白1（PAP1）是一种著名的转录因子，在植物类黄酮生物合成途径中起关键调控作用。与其他次生代谢产物类似，类黄酮生物合成表现出细胞异质性。然而，类黄酮生物合成途径的细胞特异性调控网络仍不清楚。
在本研究中，我们利用单细胞RNA测序（scRNA-seq）和时间序列代谢物谱分析来研究PAP1对拟南芥类黄酮生物合成和植物激素稳态的调控。通过比较pap1-D突变体和野生型植物叶片的单细胞转录组，我们构建了一个细胞类型特异性的基因表达图谱以及跨发育阶段代谢物的高分辨率动态变化。我们的研究结果表明，PAP1过表达在不同细胞类型中诱导苯丙烷途径基因的独特时空调控，并广泛上调糖基化过程。代谢组学分析验证了这些转录模式，并显示随着pap1-D叶片成熟，苯丙氨酸代谢过程中的代谢物发生了显著变化。此外，PAP1过表达导致植物激素水平发生显著变化，特别是茉莉酸和水杨酸，表明类黄酮生物合成与激素稳态之间存在复杂的相互作用。
这种综合的多组学方法为控制特殊代谢的细胞特异性调控网络提供了前所未有的见解，并建立了一个有价值的框架，用于优化代谢工程策略以提高生物活性植物化合物的产量。
