The Arabidopsis stomatal polarity protein BASL mediates distinct processes before and after cell division to coordinate cell size and fate asymmetries.

Yan Gong,Andrew Muroyama,Ao Liu,Dominique C Bergmann,Julien Alassimone,Rachel Varnau,Gabriel Amador

doi:10.1242/dev.199919

Abstract

ABSTRACTIn many land plants, asymmetric cell divisions (ACDs) create and pattern differentiated cell types on the leaf surface. In the Arabidopsis stomatal lineage, BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) regulates division plane placement and cell fate enforcement. Polarized subcellular localization of BASL is initiated before ACD and persists for many hours after the division in one of the two daughters. Untangling the respective contributions of polarized BASL before and after division is essential to gain a better understanding of its roles in regulating stomatal lineage ACDs. Here, we combine quantitative imaging and lineage tracking with genetic tools that provide temporally restricted BASL expression. We find that pre-division BASL is required for division orientation, whereas BASL polarity post-division ensures proper cell fate commitment. These genetic manipulations allowed us to uncouple daughter-cell size asymmetry from polarity crescent inheritance, revealing independent effects of these two asymmetries on subsequent cell behavior. Finally, we show that there is coordination between the division frequencies of sister cells produced by ACDs, and this coupling requires BASL as an effector of peptide signaling.

Highlights

Cell polarity underlies many of the asymmetric and oriented cell divisions that create daughter cells with distinct fates (Drubin and Nelson, 1996; Muroyama and Bergmann, 2019)
Loss of BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) abolishes fate asymmetry in asymmetric cell divisions (ACDs) daughter cells and disrupts patterning of the leaf epidermis To determine comprehensively the myriad functions of BASL during epidermal patterning, we re-examined the phenotypes of BASL null mutants using time-lapse imaging and whole-leaf cell lineage tracing (Gong et al, 2021a)
Our lineage tracing revealed that small cell clusters typically form from excess divisions in both the larger and smaller cells born from an ACD (Fig. 1D-F)

Summary

Introduction

Cell polarity underlies many of the asymmetric and oriented cell divisions that create daughter cells with distinct fates (Drubin and Nelson, 1996; Muroyama and Bergmann, 2019) In both plants and animals, cell polarity frequently manifests as protein enrichment in specific subdomains of the cell, often associated with the plasma. Despite similar needs for cell polarity to orchestrate cellular and developmental behaviors, plants appear to employ a different suite of polarity proteins from those used in animals One such protein, BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL), plays a central role in directing nuclear migrations to orient division planes, and in scaffolding intracellular signaling cascades to solidify differential cell fates in the Arabidopsis stomatal lineage (Dong et al, 2009; Muroyama et al, 2020; Zhang et al, 2016, 2015). The stomatal lineage features asymmetric, oriented and selfrenewing divisions (Fig. 1A) and has emerged as a powerful model for investigating how cellular polarity specifies developmental patterns in plants

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