Modulation of Asymmetric Division Diversity through Cytokinin and SPEECHLESS Regulatory Interactions in the Arabidopsis Stomatal Lineage

Coordinated growth of organs requires communication among cells within and between tissues. In plants, leaf growth is largely dictated by the epidermis; here, asymmetric and self-renewing divisions of the stomatal lineage create two essential cell types—pavement cells and guard cells—in proportions reflecting inputs from local, systemic, and environmental cues. The transcription factor SPEECHLESS (SPCH) is the prime regulator of divisions, but whether and how it is influenced by external cues to provide flexible development is enigmatic. Here, we show that the phytohormone cytokinin (CK) can act as an endogenous signal to affect the extent and types of stomatal lineage divisions and forms a regulatory circuit with SPCH. Local domains of low CK signaling are created by SPCH-dependent cell-type-specific activity of two repressive type-A ARABIDOPSIS RESPONSE REGULATORs (ARRs), ARR16 and ARR17, and two secreted peptides, CLE9 and CLE10, which, together with SPCH, can customize epidermal cell-type composition. [Display omitted] •Cytokinin promotes asymmetric spacing divisions to increase stomatal production•SPEECHLESS is an effector of CK signaling and can also induce type-A ARR16•Fine-tuning of CK signaling by cell-type-specific type A-ARRs modulates divisions•Stomatal lineage-specific peptides CLE9 and CLE10 regulate stomatal production Multicellular development requires coordination of systemic signaling with cell-type-specific outputs. Vatén et al. show how the plant hormone cytokinin interfaces with the stomatal transcription factor SPEECHLESS to modulate stem-cell-like asymmetric divisions, thus creating stomata and epidermal cells in appropriate numbers and proportions for leaf performance in fluctuating environments.