The polar code for patterning: how polarity and the cytoskeleton orchestrate asymmetric cell division during plant development

Abstract

Cell polarity is fundamental to morphogenesis across living organisms. In plants, a dynamic interplay between polarity cues and the cytoskeleton orchestrates essential asymmetric cell divisions across diverse species. Here, we focus on three functions for the cytoskeleton-organelle positioning, cell growth and mitosis-and discuss our current understanding of how polarity controls these processes. By taking a comparative approach that highlights what is known about these pathways across plant species, we spotlight both the broadly conserved and cell type-specific ways that polarity can regulate division orientation. Because there have been significant developments in the field within the last several years, we focus our attention on recent work and give our perspective on exciting future avenues of investigation into the reciprocal relationship between polarity and the cytoskeleton.

Keywords: F-actin; cell division; cytoskeleton; microtubule; plant development; polarity.

FIGURE 1

Nuclear migration and cell polarity during asymmetric cell division (ACD). (A) Following fertilization, the zygotic nucleus (dark grey) migrates toward the apical side of the cell. The zygote then undergoes an asymmetric division, producing a smaller apical cell and a larger basal cell. Disruption of F-actin using latrunculin B impairs nuclear migration, resulting in symmetric division. (B) Asymmetrically dividing cells in the Arabidopsis stomatal lineage use a cortical polarity domain defined by BASL (blue) to control two phases of nuclear migration. Before ACD, the nucleus migrates away from this domain in a microtubule-dependent manner. After division, the nucleus migrates toward the cortical polarity domain in an F-actin–dependent manner. Without BASL, directional nuclear migration is disrupted, leading to abnormal division patterns. (C) After specification, F-actin-dependent nuclear migration in lateral root founder cells is directed towards the shared cell wall. F-actin disruption results in more symmetric divisions and defective lateral root primordia. (D) A cortical polar domain classically defined by PAN1 (purple) forms at the interface between the guard mother cell (GMC) and SMC during subsidiary cell formation. The nucleus migrates toward this site in an F-actin-dependent manner. Disrupting polar domain formation in these cells leads to misoriented divisions and defective subsidiary cell formation.

FIGURE 2

Cytoskeletal rearrangement and cell polarity during asymmetric cell division. (A) Upon fertilization, F-actin (green) and microtubules (red) reorganize in the elongating zygote. This reorganization establishes a polarization axis and is important for F-actin–mediated asymmetric organelle localization. (B) Cortical BASL (blue) locally destabilizes microtubules (red) within the polar domain, preventing preprophase band (PPB) formation at this site. This ensures asymmetric inheritance of the polar domain by the stomatal lineage ground cell (SLGC) after ACD. (C) During lateral root initiation, both F-actin (green) and microtubules (red) undergo dynamic rearrangement that control asymmetric radial expansion in founder cells. (D) The localization of PAN1 (purple) excludes cortical POLAR localization (pink). In turn, POLAR blocks TAN1 localization, ensuring proper PPB (red) placement.