Single-cell transcriptomics unveils xylem cell development and evolution

The plant xylem tissue is responsible for water transportation, mechanical support and lateral growth, and can be utilized as wood. The seed plant xylem has a radial system composed of ray parenchyma cells and an axial system of fusiform cells, including tracheids in gymnosperms and vessel elements and libriform fibers in angiosperms. Little is known about the developmental programs and evolutionary relationships of these xylem cell types. Here we show that the radial and axial systems of stem-differentiating xylem are differentially conserved across four divergent woody angiosperms. Through transcriptomic profiling of single cells and cell-type regions isolated by laser capture microdissection, we identified cell types corresponding to single-cell clusters in Populus trichocarpa. Cross-species analyses of single-cell trajectories demonstrated highly conserved development in ray lineages across angiosperms. While the core eudicots P. trichocarpa and Eucalyptus grandis share nearly identical fusiform cell lineages, the tracheids in the basal eudicot Trochodendron aralioides, an evolutionarily reversed character, exhibited an expression pattern highly similar to that of vessel elements. It suggests that water transportation, instead of mechanical support, is the dominant feature of tracheary elements. Furthermore, we found that the more basal angiosperm Liriodendron chinense has a distinct fusiform lineage. This evo-developmental framework of xylem cell lineages provides a comprehensive understanding of the formation of the most abundant tissue on Earth. Single-cell RNA sequencing of stem differentiating xylem (SDX) of Populus trichocarpa, Eucalyptus grandis, Trochodendron aralioides, Liriodendron chinense. Laser capture microdissection and RNA sequencing of three xylem cell types.