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

Asymmetric and oriented stem cell divisions enable the continued production of patterned tissues. The molecules that guide these divisions include several polarity proteinsthat 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 BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (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. Dicot BASL orthologs can polarize in heterologous systems and rescue the Arabidopsis BASL mutant. The more widely distributed BASL-like proteins, although they share BASL's conserved C-terminal domain, are neither polarized nor do they function in asymmetric divisions of the stomatal lineage. Comparison of BASL protein localization and loss of function BASL phenotypes in Arabidopsis and tomato revealed 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.

Automated summary

Asymmetric and oriented stem cell divisions are crucial for the production of patterned tissues. This study identifies BASL as a eudicot-specific polarity protein that plays a major role in stomatal lineage division and cell fate asymmetries. The findings also reveal differences in how asymmetric cell divisions are used for pattern formation in different species.