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.

A hierarchical transcriptional network activates specific CDK inhibitors that regulate G2 to control cell size and number in Arabidopsis.

How cell size and number are determined during organ development remains a fundamental question in cell biology. Here, we identified a GRAS family transcription factor, called SCARECROW-LIKE28 (SCL28), with a critical role in determining cell size in Arabidopsis. SCL28 is part of a transcriptional regulatory network downstream of the central MYB3Rs that regulate G2 to M phase cell cycle transition. We show that SCL28 forms a dimer with the AP2-type transcription factor, AtSMOS1, which defines the specificity for promoter binding and directly activates transcription of a specific set of SIAMESE-RELATED (SMR) family genes, encoding plant-specific inhibitors of cyclin-dependent kinases and thus inhibiting cell cycle progression at G2 and promoting the onset of endoreplication. Through this dose-dependent regulation of SMR transcription, SCL28 quantitatively sets the balance between cell size and number without dramatically changing final organ size. We propose that this hierarchical transcriptional network constitutes a cell cycle regulatory mechanism that allows to adjust cell size and number to attain robust organ growth.