Abstract
Asymmetric and self-renewing divisions build and pattern tissues. In the Arabidopsis stomatal lineage, asymmetric cell divisions, guided by polarly localized cortical proteins, generate most cells on the leaf surface. Systemic and environmental signals modify tissue development, but the mechanisms by which plants incorporate such cues to regulate asymmetric divisions are elusive. In a screen for modulators of cell polarity, we identified CONSTITUTIVE TRIPLE RESPONSE1, a negative regulator of ethylene signaling. We subsequently revealed antagonistic impacts of ethylene and glucose signaling on the self-renewing capacity of stomatal lineage stem cells. Quantitative analysis of cell polarity and fate dynamics showed that developmental information may be encoded in both the spatial and temporal asymmetries of polarity proteins. These results provide a framework for a mechanistic understanding of how nutritional status and environmental factors tune stem-cell behavior in the stomatal lineage, ultimately enabling flexibility in leaf size and cell-type composition.
Highlights
The cellular composition of a tissue defines its structure and functions
From a genetic screen to identify regulators of cell polarity in the stomatal lineage, we found a mutation in CONSTITUTIVE TRIPLE RESPONSE (CTR1), a core component of the ethylene signaling pathway, that resulted in overall depolarization of BREVIS RADIX-LIKE 2 (BRXL2)
Live-cell imaging, lineage tracing, and quantitative image analysis of the simple, yet flexible, Arabidopsis stomatal lineage, we have been able to link ethylene and sugar signaling to the self-renewing capacity of epidermal stem cells
Summary
Tissue-embedded stem cells can control cell fate and distribution by modulating their division behaviors, often using symmetric cell divisions (SCDs) to renew stem-cell capacity and asymmetric cell divisions (ACDs) to diversify daughter cell fates (De Smet and Beeckman, 2011; Losick et al, 2011; Morrison and Kimble, 2006; Motohashi and Asakura, 2014). Tuning the relative proportion of ACDs to SCDs can modulate tissue size and organ composition in response to changes in the external and internal environment. The restricted localization of proteins, organelles, and activities to one region of the cell, is often linked to ACDs. Cell polarity can precede a division and dictate division orientation, thereby affecting daughter cell size and fate asymmetries, often through differential inheritance of specific materials (Knoblich, 2001; Muroyama and Bergmann, 2019). When the degree of polarity is not sufficient to ensure differential segregation of proteins to one daughter, it can trigger a developmental switch from ACDs to SCDs
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