Polarity in plant asymmetric cell division: Division orientation and cell fate differentiation

Abstract

Asymmetric cell division (ACD) is universally required for the development of multicellular organisms. Unlike animal cells, plant cells have a rigid cellulosic extracellular matrix, the cell wall, which provides physical support and forms communication routes. This fundamental difference leads to some unique mechanisms in plants for generating asymmetries during cell division. However, plants also utilize intrinsically polarized proteins to regulate asymmetric signaling and cell division, a strategy similar to the differentiation mechanism found in animals. Current progress suggests that common regulatory modes, i.e. protein spontaneous clustering and cytoskeleton reorganization, underlie protein polarization in both animal and plant cells. Despite these commonalities, it is important to note that intrinsic mechanisms in plants are heavily influenced by extrinsic cues. To control physical asymmetry in cell division, although our understanding is fragmentary thus far, plants might have evolved novel polarization strategies to orientate cell division plane. Recent studies also suggest that the phytohormone auxin, one of the most pivotal small molecules in plant development, regulates ACD in plants.

Keywords: Asymmetric cell division; Auxin signaling; Cell division orientation; Cell polarity; Differential cell identity; Plant development; Protein polarization.

Fig 1

Symmetry-breaking polarization of Cdc42 and BASL in yeast and Arabidopsis stomatal lineage cells. (A) Left panel: Spontaneous polarization of the Cdc42-Bem1-Cdc24/PAK feedforward loop. In budding yeast, stochastically activated Cdc42-GTP (gray arrow) recruits the scaffold protein Bem1, which locally enrich Cdc24 the Cdc42 GEF activator, to amplify activated Cdc42-mediated protein clustering. This intrinsic positive feedback loop polarizes Cdc42 to the cortical site and promotes daughter cell expansion (black arrow). Right panel: In Arabidopsis stomatal ACD precursor cells, a positive feedback loop of BASL-YDA-MAPK3/6 promotes cell polarization. MPK3/6-mediated phosphorylation triggers BASL cortical polarization (gray arrow). At the cell cortex, phosphorylated BASL functions as a scaffold to recruit both YDA and MPK3/6, which further produces more activated MPK3/6, and thus more activated BASL to polarize. Polarization of the BASL complex was hypothesized to promote local cell expansion (black arrow) (B)Working model for spontaneous clustering of BASL-YDA-MPK3/6 in plant cells. We hypothesize that, similar to Cdc42 polarization, initially activated BASL molecules organize a positive feedback loop by recruiting its activators YDA-MPK3/6, which allows the conversion of neighboring molecules to become active, eventually leading to the formation of a polarized cluster.

Fig 2

Actin-dependent positive feedback loops for symmetry-breaking polarization in yeast and maize stomatal cells. (A) Cytoskeletal-dependent polarization of Cdc42 in yeast. Cortically localized active Cdc42-GTP triggers Formin activity (bundling factor) to form actin cables. Actin cables provide tracks for the delivery of exocytotic vesicles carrying Cdc42-GTP to the polarizing site, resulting in further nucleation of actin cables, which in turn enhances the Cdc42 polar enrichment (dashed arrows). Blue arrow shows the moving direction of Cdc42-GTP vesicles driven by actin motor proteins. The formation of actin patches is stimulated by Cdc42-GTP activated SCARE/WAVE and Arp2/3, which promote actin nucleation and branching. Actin patches are necessary for dynamic delivery of PM and cell wall materials. (B)PAN1/2 polarization in maize Subsidiary Mother Cells (SMCs). In SMC, polarized PAN1/2 physically bind to ROP and lead to ROP activation. Polarized ROP activates the SCAR/WAVE and Arp2/3 activity and thus nucleation of actin to form a dense actin patch at the polarity site. Actin patches may help directional nuclear migration (black arrow) during SMC ACD. Interestingly, polarization of SCAR/WAVE is also required for PAN1/2 polarization, suggesting an interdependent activation (dashed arrows).

Fig 3

A hypothetical MAPK gradient and asymmetric placement of cell division plane in the Arabidopsis stomatal lineage. In Arabidopsis stomatal ACD, we hypothesize that the YDA MPK3/6 signaling forms a gradient. Two possible mechanisms may contribute to this gradient. The positive feedback loop with BASL maintains a high concentration of MPK3/6 at the crescent. Extrinsic peptide ligands EPF1/2, derived from the neighboring stomatal cells, are perceived by the membrane receptors TMM and ERECTA family, which may locally activate the downstream YDA-MPK3/6 pathway. The formation of the PPB requires a core TTP complex containing protein phosphatase PP2A enzymes with two MT-binding proteins, TON1 and TRM. The PPB-associated MT regulators, e.g. MOR1, CLASP1 and EB1, might be subject to MAPK- and PP2A-mediate phosphorylation and dephosphorylation, respectively, to initiate and orientate the PPB formation.

Fig 4

Auxin signaling participates in plant ACD. (A) Auxin pathway promotes ACD in early embryos. In 8-cell embryos, ACDs were detected in the lower tier (purple) by 3D high-resolution confocal imaging and computational analyses. The volume of outer cells (protoderm) is about two times that of the inner cells (precursor of vasculature and ground tissues). However, in the auxin inhibitor mutant bdl/iaa12, ACDs were reverted to symmetric. How auxin signaling promotes asymmetric placement of the division plane is unknown. (B)Auxin depletion from the M is linked to stomatal differentiation after an ACD. In the wild-type (WT), auxin level drops when the M differentiates into stomatal guard cells. Auxin depletion is likely mediated by elevated expression level of the PIN3 auxin effluxer (purple). In the loss-of-function mutant pin1 3 4 7, the M maintains high level of auxin and does not differentiate, but divide more times before terminal fate adoption.

Fig 5

Asymmetrically activated MAPK signaling in muscle satellite cell ACD and Arabidopsis stomatal ACD. (A) Asymmetric p38α/β MAPK activity in mouse muscle satellite cell ACD. Polarized PAR protein complex activates p38α/β MAPK activity in only one daughter cell, which turns on the expression of bHLH transcription factor MyoD to promote amplifying divisions followed by terminal fate differentiation. The other daughter cell exits cell division and returns to the quiescent state. (B)Asymmetric distribution of the YDA-MPK3/6 cascade in Arabidopsis stomatal ACD. Premitotically polarized BASL-YDA-MPK3/6 complex is only inherited to the large daughter cell (SLGC, stomatal lineage ground cell), which results in phosphorylation of the nuclear bHLH SPCH for degradation. Differential SPCH expression levels in two daughters direct their distinct developmental path. The small daughter (M, Meristemoid) undergoes a few divisions and terminates into stomatal guard cells and the large SLGC expands to become a pavement cell (PC).