Single-cell and spatial multiomics identifies heterogeneous xylem development driven by mechanical stress in Populus

Abstract

Xylem, the predominant tissue for structural support, forms tension wood with G-layer-rich fibers under mechanical stress. Despite being recognized over a century ago, three key biological questions remained unclear: (1) are fibers in normal and tension wood distinct cells due to morphological differences? (2) Do tension wood fibers arise from different lineages? (3) What are the key genes controlling tension wood formation? We conducted single-cell RNA sequencing on normal, tension and opposite xylem. Fibers in normal and tension wood belong to the same cell type and lineage. Differential developmental speed and cell-type ratio in tension and opposite xylem were further validated by spatial transcriptomics and metabolomics. Phosphoproteomics showed mechanical sensing mechanisms conserved between stems and roots across angiosperms. We identified a group of genes involved in the cell fate transition in tension wood. The knowledge on the heterogeneity of cell development offers insights into optimizing biomass production and bioenergy yield.