A Spatiotemporal Molecular Switch Governs Plant Asymmetric Cell Division

Abstract

SummaryAsymmetric cell division (ACD) often requires protein polarization in the mother cell to produce daughter cells with distinct identities (“cell-fate asymmetry”). Here, we define a previously undocumented mechanism for establishing cell-fate asymmetry in Arabidopsis stomatal stem cells. In particular, we show that polarization of BSL protein phosphatases promotes stomatal ACD by establishing a “kinase-based signaling asymmetry” in the two daughter cells. BSL polarization in the stomatal ACD mother cell is triggered upon commitment to cell division. Polarized BSL is inherited by the differentiating daughter cell where it suppresses cell division and promotes cell-fate determination. Plants lacking BSL exhibit stomatal over-proliferation, demonstrating BSL plays an essential role in stomatal development. Our findings establish that BSL polarization provides a spatiotemporal molecular switch that enables cell-fate asymmetry in stomatal ACD daughter cells. We propose BSL polarization is triggered by an ACD “checkpoint” in the mother cell that monitors establishment of division-plane asymmetry.

Opposite polarity programs regulate asymmetric subsidiary cell divisions in grasses

“…In Arabidopsis, AtPOLAR interacts and sequesters the GSK3-like kinase BIN2 that prohibits it from inhibiting the transcription factor SPEECHLESS (SPCH) (Houbaert et al, 2018), which establishes stomatal identity and regulates stomatal ACDs (MacAl-ister et al, 2007). Right at the onset of mitosis, a BSL family phosphatase is recruited to the polarity crescent in meristemoids, which releases BIN2 (Guo et al, 2021b). This enables BIN2 to enter the nucleus, downregulate SPCH and inhibit ACD potential in the larger daughter cell (Guo et al, 2021b; Houbaert et al, 2018).…”

Using quantitative methods to understand leaf epidermal development

“…While this interaction is disrupted after asymmetric cell division, BIN2 relocates to the nucleus to destabilise SPCH in SLGCs, leading to asymmetric cell fates (Guo & Dong, 2019; Houbaert et al, 2018). Besides BIN2, recent work on the BRI1 SUPPRESSOR1-LIKE (BSL) family of protein phosphatases has also revealed that the spatial modulation of MAPK signalling at the subcellar level is key for asymmetric fate acquisition (Guo et al, 2021; 2022).…”

Establishing asymmetry: stomatal division and differentiation in plants

“…Consequently, the BIN2‐mediated inhibition of YDA is released, whilst nuclear BIN2 may directly bind and phosphorylate SPCH for degradation (Gudesblat et al ., 2012). On the other hand, polarized BSL1 directly binds to YDA for dephosphorylation and activation, leading to elevated MAPK signaling and further suppressed SPCH (Guo et al ., 2021). Therefore, through the joint regulation of BIN2 (translocation) and YDA (activation), the assembly of BSL1 in the polarity complex, upon the MMC entry to mitosis, can quickly lower the protein level of SPCH and tune down the division potential of MMC, thereby enabling the progression towards SLGC in stomatal ACD (Guo et al ., 2021).…”

“…Then, the next question was how the inhibition of BIN2 on YDA can be alleviated after division in SLGC. Recently, members of the BRI1 SUPPRESSOR (BSU1) family were identified to interact with BASL and the founding member BSL1 joins the polarity site and functions as a molecular switch to enable the transition from MMC to SLGC (Guo et al ., 2021). Time‐lapse examination of fluorescent protein‐tagged BSL1 showed that BSL1 becomes polarized slightly later than BASL in MMC and coincides with the formation of the preprophase band (an indication of the entry to mitosis) (Fig.…”