Establishing cell polarity in plants: the role of cytoskeletal structures and regulatory pathways

Abstract

Cell polarity is a fundamental mechanism of plant cells that drives cellular specialization and the formation of diverse cell types. It regulates critical developmental events, including polarized tip growth (such as pollen tubes and root hairs), epidermal patterning (such as trichome branching and asymmetric cell division in stomata). The establishment and maintenance of cell polarity rely on the cytoskeleton-mediated polarized distribution of specific proteins and organelles. In particular, cell-type-specific actin and microtubule dynamic structures are pivotal for maintaining polarity. For example, actin cables and short actin fragments are critical for pollen tube growth, while actin clusters and microtubule rings are involved in trichome branching, and actin patches contribute to stomatal mother cell polarization. Beyond directing the polarization of organelles and proteins, the cytoskeleton itself serves as an intrinsic cue for polarity. For instance, actin patches in stomatal precursor cells act as self-organizing polarity landmarks. Despite the diversity of cytoskeletal structures and their functions, common regulators, such as Rop GTPase signaling pathways, WAVE/SCAR complexes, and motor proteins regulate the assembly and function of these structures. Recent advances have revealed new regulatory mechanisms, such as microtubule exclusion zones guiding asymmetric divisions during Arabidopsis stomatal development, and the role of actin rings in regulating xylem pit formation. These discoveries contribute to a deeper understanding of the cytoskeleton's crucial role in polarity regulation. In this review, we highlight the key cytoskeletal structures involved in the establishment of cell polarity in plants and discuss the molecular mechanisms underlying their spatiotemporal assembly. We also address emerging questions regarding the cytoskeleton's role in cell polarity and development.

Keywords: actin; cell polarity; microtubule; polarity proteins; polarity regulation.

FIGURE 1

Dynamics of actin filaments and microtubules in tip growth. (A) In pollen tubes, actin filaments (AFs) and microtubules (MTs) exhibit distinct organizational dynamics in different regions. These specific cytoskeletal arrangements enable pollen tubes to coordinate vesicle transport, cell wall formation, and the rapid establishment of polarity during tip growth. Moss protonemal cells, on the other hand, possess a unique cytoskeletal organization, further emphasizing the diversity of cytoskeletal architectures among different tip-growing cell types. Additionally, the polar localization of ROP1/PpBrk1 plays a critical role in tip growth. (B) During rice pollen germination, both AFs and MTs form radial patterns radiating from the germination pore. (C) Root hairs represent another form of tip growth. A core function of AFs in root hairs is transporting membrane compartments to the root tip, thereby delivering cell wall components and membrane lipids required for apical growth. MTs play a crucial role in maintaining the directional growth of root hairs. In growing Arabidopsis root hairs, ROP2 localizes to the root hair tip.

FIGURE 2

Dynamics of actin filaments and microtubules during diffuse growth. (A) During the formation of trichomes in Arabidopsis thaliana, actin filaments (AFs) form an actin network at the tip, while microtubules (MTs) form transverse rings. (B) In the formation of pavement lobes, AFs and MTs also exhibit distinct dynamic distributions. Cortical fine AFs localize to the top of the lobe outgrowth, whereas MTs are arranged transversely in the neck region of lobes. In pavement cells (PCs), two antagonistic ROP pathways (ROP2- and ROP6-GTPase pathways) cooperatively regulate lobe morphogenesis. The ROP2-RIC4 interaction drives lobe outgrowth by promoting actin assembly, whereas the ROP6-RIC1 interaction restricts lobe expansion through microtubule organization. PM, plasma membrane. (C) During pit formation in xylem cells, AFs and MTs regulate cell wall deposition as well as the size and aperture of pits. ROP domains coordinate secondary cell wall patterning. Active ROP11 (activated by ROPGEF4/ROPGAP3) recruits MIDD1 and kinesin-13A to pit domains, creating microtubule-free zones that suppress wall deposition.

FIGURE 3

Dynamics of actin filaments and microtubules in asymmetric cell division. (A) Schematic of microtubules (MTs) and actin filaments (AFs) dynamics during zygote polarization. AFs are essential for nuclear positioning and division plane establishment, while MT ring demarcate the subapical domain and promotes apical-directed cell expansion. (B) Schematic of Arabidopsis stomatal lineage divisions. Two oppositely oriented nuclear movements, NMpre (pre-division) and NMpost (post-division), are shown during the asymmetric division of the stomatal meristemoid mother cell (MMC). The nuclear color darkens at later time points. Additionally, the polar localization of BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) and BREVIS RADIX family (BRXf) plays a critical role in stomatal patterning.(C) Schematic of stomatal development in maize. In the asymmetric division of subsidiary mother cells (SMCs), the establishment of cellular polarity guides both the proper distribution of the cytoskeleton and the determination of asymmetric division orientation. (D) Schematic of asymmetric division in the protonemal subapical cell (SA) of the moss Physcomitrium patens. During preprophase/prophase, the SA assembles an apical actin patch (green) and protrudes the membrane to form a bulge (indicated by a gray arrow). The nucleus migrates into the bulge, followed by nuclear envelope disassembly and mitotic spindle formation.