Abstract
The presumed totipotency of plant cells leads to questions about how specific stem cell lineages and terminal fates could be established. In the Arabidopsis stomatal lineage, a transient self-renewing phase creates precursors that differentiate into one of two epidermal cell types, guard cells or pavement cells. We found that irreversible differentiation of guard cells involves RETINOBLASTOMA-RELATED (RBR) recruitment to regulatory regions of master regulators of stomatal initiation, facilitated through interaction with a terminal stomatal lineage transcription factor, FAMA. Disrupting physical interactions between FAMA and RBR preferentially reveals the role of RBR in enforcing fate commitment over its role in cell-cycle control in this developmental context. Analysis of the phenotypes linked to the modulation of FAMA and RBR sheds new light on the way iterative divisions and terminal differentiation are coordinately regulated in a plant stem-cell lineage.
Highlights
Plants exhibit remarkable developmental plasticity and their cells are typically considered totipotent, in that a complete plant can be regenerated from nearly any isolated individual cell
Mosaic co-suppression of the RBRp:RBR-CFP transgene leads to loss of fluorescence and concomitant excessive divisions in the CFP-minus sectors, suggesting that RBR represses cell divisions in both the early lineage and the terminally differentiated guard cells (GCs) (Figure 1D)
FAMALGK plants (FAMAp):artificial microRNAs (amiRNAs)-RBR GCs underwent inappropriate extra divisions oriented transverse to the long axis of the cells, while other epidermal cells were not affected, confirming a direct requirement for RBR in GCs (Figure 1E and Figure 1—figure supplement 1A) and confirming phenotypes reported using different amiRNAs directed against RBR (Lee et al, 2014a)
Summary
Plants exhibit remarkable developmental plasticity and their cells are typically considered totipotent, in that a complete plant can be regenerated from nearly any isolated individual cell. At the end of their renewing stages, these meristemoids differentiate into guard mother cells (GMCs), which undergo a single symmetric division to generate the paired guard cells (GCs) of the mature stomata. GCs and each of the intermediate stages leading to their formation are characterized by distinct morphologies and unique gene expression profiles, allowing experimental dissection of lineage progression in intact, developing organs (Lau and Bergmann, 2012; Pillitteri and Dong, 2013). The basic helix-loop-helix (bHLH) transcription factor FAMA is a master regulator of guard cell identity; it is necessary and sufficient for GC fate acquisition and its epidermal expression is limited to GMCs and young GCs (Ohashi-Ito and Bergmann, 2006) and (Figure 1B). Overexpression of FAMA reprograms other cells into GC identity, while simultaneously repressing cell division to yield
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