On the edge: Evolution of polarity protein BASL and the capacity for stomatal lineage asymmetric divisions

ABSTRACT Asymmetric and oriented stem cell divisions enable the continued production of patterned tissues. The molecules that guide these divisions include several “polarity proteins” that are localized to discrete plasma membrane domains, are differentially inherited during asymmetric divisions, and whose scaffolding activities can guide division plane orientation and subsequent cell fates. In the stomatal lineages on the surfaces of plant leaves, asymmetric and oriented divisions create distinct cell types in physiologically optimized patterns. The polarity protein BASL is a major regulator of stomatal lineage division and cell fate asymmetries in Arabidopsis, but its role in the stomatal lineages of other plants is unclear. Here, using phylogenetic and functional assays, we demonstrate that BASL is a eudicot-specific polarity protein. Among dicots, divergence in BASL’s roles may reflect some intrinsic protein differences, but more likely reflects previously unappreciated differences in how asymmetric cell divisions are employed for pattern formation in different species. This multi-species analysis therefore provides insight into the evolution of a unique polarity regulator and into the developmental choices available to cells as they build and pattern tissues. HIGHLIGHTS BASL is a eudicot-specific regulator of stomatal lineage asymmetric cell divisions BASL protein evolution includes stepwise addition of polarity domains to an ancestral MAPK-binding chassis Cellular quiescence and BASL-guided polarity generate proper stomatal spacing in tomato Cell size and fate asymmetries are uncoupled in the tomato stomatal lineage