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单细胞核转录组分析揭示油菜种皮分化过程和种子颜色差异原因

巨建业1,2,杨柳1,2,陈浩1,2,康雷1,2,夏石头3,刘忠松1,2,*   

  1. 1 湖南农业大学农学院, 湖南长沙 410128; 2 岳麓山实验室, 湖南长沙 410128; 3 湖南农业大学 / 植物激素与生长发育湖南省重点实验室, 湖南长沙 410128
  • 收稿日期:2025-05-07 修回日期:2025-08-13 接受日期:2025-08-13 网络出版日期:2025-08-26
  • 基金资助:
    本研究由国家自然科学基金项目(U20A2029)和湖南省科技创新计划项目(2022RC1144)资助。

Single-nucleus transcriptome analysis reveals the cellular differentiation trajectories and molecular mechanisms underlying yellow seed coat formation in rapeseed

JU Jian-Ye1,2,YANG Liu1,2,CHEN Hao1,2,KANG Lei1,2,XIA Shi-Tou3,LIU Zhong-Song1,2,*   

  1. 1 College of Agronomy, Hunan Agricultural University, Changsha 410128, Hunan, China; 2 Yuelu Mountain Laboratory, Changsha 410128, Hunan, China; 3 Hunan Agricultural University / Hunan Provincial Key Laboratory of Phytohormones, Changsha 410128, Hunan, China
  • Received:2025-05-07 Revised:2025-08-13 Accepted:2025-08-13 Published online:2025-08-26
  • Supported by:
    This study was supported by the National Natural Science Foundation of China (U20A2029) and the Science and Technology Innovation Program of Hunan Province (2022RC1144).

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摘要：

被子植物的种皮由多层结构和功能各异细胞组成，不同层细胞表达的基因及其表达特征尚不完全明确，并且这些具有特定功能的细胞层分化过程仍有待阐明。黄籽油菜比黑籽油菜种皮薄、无色素、木质素含量低，但是导致种皮差异的原因仍需进一步研究。本研究以甘蓝型黄籽油菜黄矮早和黑籽油菜中双11号为材料，取开花后25 d的种皮用单细胞核转录组测序技术绘制单细胞转录图谱，结合拟时序、基因表达差异、基因共表达网络和细胞通讯分析，解析种皮发育分化过程和种子颜色差异的原因。结果表明，可以将甘蓝型油菜种皮分为7个细胞亚群，STK基因调控合点端种皮分化先后形成远端种皮OI3、OI2和OI1层外种皮以及II1和II2层内种皮。与黑籽相比，黄籽II1层原花色素合成基因、OI1层木质素和黄酮醇合成基因、OI3层黏液合成相关基因的表达均显著下调，而II2层核苷酸和氨基酸代谢相关基因、OI2和OI3淀粉合成相关基因的表达均显著上调。转录因子编码基因TT8和酶编码基因TT3、TT18以及转运蛋白编码基因TT12在II1层共表达调控PA的合成，同时TT19催化PA与GSH结合增强其水溶性，而TT10参与PA单体的氧化聚合，最终由TT12和TT9介导修饰后PA的转运。本研究是首次对植物种皮进行单细胞测序分析，并揭示了油菜种皮不同细胞群的分化过程和原花色素、木质素和淀粉的细胞分布和积累时期，从细胞水平阐明了黄籽形成的分子机制。

关键词: 甘蓝型油菜, 单细胞核转录组, 种皮, 种子颜色, 类黄酮代谢

Abstract:

The seed coat of angiosperms consists of multiple layers of cells with distinct structures and functions. However, the specific gene expression profiles within each layer and their spatial-temporal patterns remain incompletely characterized, and the differentiation pathways leading to these functionally specialized layers are not yet fully understood. Compared to black-seeded rapeseed, yellow-seeded varieties exhibit a thinner seed coat, reduced pigmentation, and lower lignin content. The exact cell layers responsible for these phenotypic differences, however, have not been clearly identified. In this study, we used the yellow-seeded rapeseed variety “Huangaizao” and the black-seeded variety “Zhongshuang 11” as experimental materials. Seed coats were collected at 25 days after flowering and subjected to single-nucleus RNA sequencing to construct a high-resolution single-cell transcriptional atlas. By integrating pseudotime trajectory analysis, differential gene expression profiling, weighted gene co-expression network analysis (WGCNA), and PlantPhoneDB-based cell–cell communication analysis, we investigated the regulatory networks and intercellular signaling mechanisms involved in seed coat development and seed color differentiation. Our results revealed that the yellow-seeded rapeseed seed coat comprises seven distinct cell subpopulations. The STK gene orchestrates the ordered differentiation of distal and proximal seed coat layers, giving rise to the outer layers OI3, OI2, and OI1, as well as the inner layers II1 and II2. Compared to black-seeded rapeseed, genes involved in flavonoid biosynthesis (in II1), lignin and flavonol synthesis (in OI1), and mucilage synthesis (in OI3) were significantly downregulated in yellow-seeded rapeseed. In contrast, genes related to nucleotide and amino acid metabolism (in II2), as well as starch biosynthesis (in OI2 and OI3), were significantly upregulated. Within the II1 layer, the transcription factor TT8, together with the enzyme-coding genes TT3 and TT18, and the transporter gene TT12, were co-expressed to regulate proanthocyanidin (PA) biosynthesis. Concurrently, TT19 catalyzed the conjugation of PA with glutathione (GSH), enhancing its water solubility, while TT10 mediated the oxidative polymerization of PA monomers. Finally, the modified PAs were transported by TT12 and TT9. To our knowledge, this study represents the first single-cell transcriptomic analysis of plant seed coats. It unveils the differentiation trajectories of specific cell types in the rapeseed seed coat and elucidates the spatial and temporal dynamics of PA, lignin, and starch accumulation at single-cell resolution. These findings offer novel insights into the molecular mechanisms underlying yellow seed formation from a single-cell perspective.

Key words: Brassica napus L., single-nucleus transcriptome, seed coat, seed color, flavonoid metabolism

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