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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: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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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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