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

Symmetric tissue alignment is pivotal to the functions of plant vascular tissue, such as long-distance molec-ular 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 symme-try 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 compres-sive stress, smoothing, and symmetrizing cell arrangement of the vascular-cell-type boundary. Mechanisti-cally, 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 me-chanical stress to the position distal and symmetric to the boundary. By combinatorial analyses of mechan-ical 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 mech-anism controlling the boundary alignment and symmetry in tissue lacking cell fluidity.

Automated summary

Cell proliferation and cytokinin signaling play important roles in maintaining the symmetry of vascular tissue in plants. The GATA transcription factor and Arabidopsis response regulators cooperatively regulate cell proliferation to generate mechanical stress, which in turn shapes the symmetry and alignment of vascular tissue. This mechanism represents an alternative way to control tissue symmetry in the absence of cell fluidity.