Patterned proliferation orients tissue-wide stress to control root vascular symmetry in Arabidopsis

Symmetric tissue alignment is pivotal to the functions of plant vascular tissue, such as long-distance molecular transport and lateral organ formation. During the vascular development of the Arabidopsis roots, cytokinins initially determine cell-type boundaries among vascular stem cells and subsequently promote cell proliferation to establish vascular tissue symmetry. Although it is unknown whether and how the symmetry of initially defined boundaries is progressively refined under tissue growth in plants, such boundary shapes in animal tissues are regulated by cell fluidity, e.g., cell migration and intercalation, lacking in plant tissues. Here, we uncover that cell proliferation during vascular development produces anisotropic compressive stress, smoothing, and symmetrizing cell arrangement of the vascular-cell-type boundary. Mechanistically, the GATA transcription factor HANABA-TARANU cooperates with the type-B Arabidopsis response regulators to form an incoherent feedforward loop in cytokinin signaling. The incoherent feedforward loop fine-tunes the position and frequency of vascular cell proliferation, which in turn restricts the source of mechanical stress to the position distal and symmetric to the boundary. By combinatorial analyses of mechanical simulations and laser cell ablation, we show that the spatially constrained environment of vascular tissue efficiently entrains the stress orientation among the cells to produce a tissue-wide stress field. Together, our data indicate that the localized proliferation regulated by the cytokinin signaling circuit is decoded into a globally oriented mechanical stress to shape the vascular tissue symmetry, representing a reasonable mechanism controlling the boundary alignment and symmetry in tissue lacking cell fluidity. [Display omitted] •Xylem-procambium boundary is refined with vascular tissue growth•HANABA-TARANU/cytokinin circuit fine-tunes the proliferation position and frequency•Biased vascular proliferation orients compressive stress among vascular cells•Proliferation-induced stress symmetrizes and smoothens less fluidic tissue boundary How is the symmetry of a multicellular organ elaborated in a plant? Fujiwara et al. show that cytokinin-directed patterned proliferation produces coherently oriented mechanical stress during vascular tissue growth in Arabidopsis roots. This tissue-wide stress field efficiently symmetrizes the arrangement of immobile cells, refining organ symmetry.