Arabidopsis stomatal lineage cells establish bipolarity and segregate differential signaling capacity to regulate stem cell potential.

Cell polarity combined with asymmetric cell divisions (ACDs) generates cellular diversity. In the Arabidopsis stomatal lineage, a single cortical polarity domain marked by BASL orients ACDs and is segregated to the larger daughter to enforce cell fate. We discovered a second, oppositely positioned polarity domain defined by OCTOPUS-LIKE (OPL) proteins, which forms prior to ACD and is segregated to the smaller (meristemoid) daughter. Genetic and misexpression analyses show that OPLs promote meristemoid-amplifying divisions and delay stomatal fate progression. Polarity mediates OPL segregation into meristemoids but is not required for OPL function. OPL localization and activity are largely independent of other stomatal polarity genes and of the brassinosteroid signaling components associated with OPLs in other contexts. While OPLs are unique to seed plants, ectopic expression in the liverwort Marchantia suppressed epidermal fate progression, suggesting that OPLs engage ancient and broadly conserved pathways to regulate cell division and cell fate.