Cortical polarity ensures its own asymmetric inheritance in the stomatal lineage to pattern the leaf surface

Asymmetric cell divisions specify differential cell fates across kingdoms. In metazoans, preferential inheritance of fate determinants into one daughter cell frequently depends on polarity-cytoskeleton interactions. Despite the prevalence of asymmetric divisions throughout plant development, evidence for analogous mechanisms that segregate fate determinants remains elusive. Here, we describe a mechanism in the Arabidopsis leaf epidermis that ensures unequal inheritance of a fate-enforcing polarity domain. By defining a cortical region depleted of stable microtubules, the polarity domain limits possible division orientations. Accordingly, uncoupling the polarity domain from microtubule organization during mitosis leads to aberrant division planes and accompanying cell identity defects. Our data highlight how a common biological module, coupling polarity to fate segregation through the cytoskeleton, can be reconfigured to accommodate unique features of plant development.

Automated summary

Asymmetric cell divisions play a crucial role in determining cell fates in different kingdoms. While animal cells rely on polarity-cytoskeleton interactions, little is known about the mechanisms segregating fate determinants during asymmetric divisions in plants. This study uncovers a mechanism in Arabidopsis leaf epidermis that ensures unequal inheritance of a fate-enforcing polarity domain. The polarity domain limits division orientations by depleting stable microtubules in a specific cortical region, and disruption of this mechanism results in aberrant division planes and cell identity defects.