Single-cell spatiotemporal transcriptomics reveals the origin, cellular heterogeneity and regulatory network of seed fiber cells in poplar

Poplar (Populus spp.) is globally important for timber and afforestation, and is also a model system for woody perennials. However, the molecular control of reproductive organ development, particularly that of the epidermal trichomes on seeds known as seed fibers (fluff), which cause environmental and health concerns, remains poorly understood. Here, integrating single-nucleus RNA sequencing (snRNA-seq) with spatial transcriptomics, we constructed a spatiotemporal atlas of female poplar capsules that resolves the cellular composition of the organ and positions each cell type within its native tissue context. We traced the developmental trajectory of seed fibers, showing that they originate from placenta epidermal cells, and identified three functionally distinct fiber cell subtypes involved in initiation, photosynthesis and elongation. Network analysis identified candidate regulators including PtoPDF2, PtoMYB38 and PtoHDG11. PtoPDF2 activates PtoMYB38 and PtoSTK2 by binding L1-box motifs in their promoters, revealing a module that governs seed fiber initiation. Together, our study provides a framework for seed fiber development in poplar and candidate targets for breeding low-fluff cultivars.