Asymmetric cell division in plants: mechanisms of symmetry breaking and cell fate determination

Abstract

Asymmetric cell division is a fundamental mechanism that generates cell diversity while maintaining self-renewing stem cell populations in multicellular organisms. Both intrinsic and extrinsic mechanisms underpin symmetry breaking and differential daughter cell fate determination in animals and plants. The emerging picture suggests that plants deal with the problem of symmetry breaking using unique cell polarity proteins, mobile transcription factors, and cell wall components to influence asymmetric divisions and cell fate. There is a clear role for altered auxin distribution and signaling in distinguishing two daughter cells and an emerging role for epigenetic modifications through chromatin remodelers and DNA methylation in plant cell differentiation. The importance of asymmetric cell division in determining final plant form provides the impetus for its study in the areas of both basic and applied science.

Keywords: Asymmetric cell division; Cell fate determination; Cell polarity; Plant development; Stem cells.

Fig. 1

Intrinsic and extrinsic pathways determine asymmetric cell fate in animals and plants. a An intrinsic polarity pathway in animals is represented by PAR proteins that are differentially segregated (orange and green) in one cell stage C. elegans embryos. A anterior, P posterior. Polarized PAR proteins induce unequal degradation of the PIE-1 differentiating transcription factor. Arrows indicate positive regulation and blocked lines indicate negative regulation. b The organization of stem cell niche (SCN) in Drosophila female germ lines. Secreted morphogenes (BMP) from cap cells are perceived by the receptors (Tkv/Punt) in stem cells to inhibit the expression of the differentiation gene Bam. The expression of Bam in the daughter cells outside of the niche drive fate differentiation. c The intrinsic polarity pathway in plants is represented by the BASL polarity module in stomatal asymmetric division in Arabidopsis. The polarity complex is composed of BASL, the MAPKKK YDA, MPK3/6 and POLAR and is inherited in the stomatal lineage ground cell (SLGC) but not the meristemoid (M). Extrinsic signals (arrowhead) are hypothesized to trigger BASL polarization through the YDA MAPK pathway. The SPCH transcription factor is a direct substrate of MAPK for degradation. An unequal expression of SPCH is therefore hypothesized to associate with the BASL polarity complex. d The organization of stem cell niche in Arabidopsis root apical meristem. The WOX5 transcription factors in the quiescent center maintains the neighboring stem cell via the ACR4 receptor, which delivers CLE40 signals from the differentiating columella cells, to suppress WOX5 expression. The negative feedback loop between WOX5 and ACR4 maintains stem cell homeostasis in the root

Fig. 2

Mobile factors control division and cell fate decisions. a Columella stem cell division. WOX5 moves from the QC (quiescent center) to the columella SC (stem cell). FEZ expression dynamically oscillates during rounds of asymmetric division. FEZ activates SMB in differentiating columella to produce a feedback loop to ultimately inhibit the expression of FEZ in the CC (columella cell). b Division of endodermis/cortex initials. Cell types are color coded as indicated. The diffusible transcription factor SHR moves from the stele to the endodermis where it is sequestered by SCR. SHR movement into the cortex is prevented and a positive feedback loop promotes endodermal cell fate. c Hypophysis division. MP activates TMO7 in provasculature (orange), which moves to the hypophysis (dark green). MP activation results in basally directed auxin flow through the up-regulation of PIN1. Both auxin response and TMO7 activity is necessary to specify hypophysis identity and initiate division

Fig. 3

Auxin and cell wall components in asymmetric cell division. a Zygotic asymmetric division. WRKY2 promotes zygotic elongation and activation of WOX8/9 that is required for WOX2 expression in the apical domain. Increased level of auxin in the apical cell is mediated by PIN7 activity. In tobacco zygotic division, AGPs are enriched in the apical cell. In Arabidopsis, the YDA MPK3/6 cascade transmits the upstream SSP and ESF1 signaling to the downstream transcription factor GRD to promote zygotic elongation and asymmetric division. GRD is not a direct substrate of MPK3/6 (dashed arrow) and may function with an unknown partner (question mark) downstream of the YDA MPK3/6 cascade. b SPCH initiates stomatal asymmetric division of the meristemoid mother cell (MMC) to produce a small daughter cell meristemoid (M) and a large daughter cell, stomatal lineage ground cell (SLGC). After a few rounds of M asymmetric division (arrow), MUTE expression turns on guard cell (GC) differentiation. High auxin level is associated with stomtal asymmetric division and auxin depletion is mediated by PIN3 in Ms and is associated with GC differentiation. The negative regulation of auxin on stomatal production is achieved by TIR1/AFB-mediated suppression of a positive regulator Stomagen

Fig. 4

Epigenetic regulations in stem cell asymmetric cell division in Arabidopsis. a Histone modification events in the root stem cell niche. The SWI/SNF remodeling ATPase BRM directly interacts with the chromatin regions of PIN1, 2, 3, 4, 7 to promote their expression by suppressing the polycomb group (PcG) protein binding, which deposits the repressing mark H3K27me3. The expression of WOX5 is positively regulated by SDG2, a TrxGH3K4-methyltransferases, that marks the chromatin region with activating H3K4me3. b Active DNA methylation and histone modification in stomatal fate differentiation. The expression of EPF2 peptide is suppressed by the RdDM pathway-induced DNA methylation in the promoter region of EPF2, which is actively erased by the ROS1 DNA glycosylase. The terminal differentiation of guard cells is secured by the FAMA-RBR complex that suppresses the expression of stomatal early genes (SPCH and others). RBR can recruit the PcG proteins that deposit H3K27me3 repressive marks to the FAMA-binding regions