The patterning of epidermal cell types in Arabidopsis is a simple and useful model for studying the molecular basis of cell specification in plants. The distribution of different cell types in the Arabidopsis epidermis is regulated by a lateral inhibition mechanism that relies on interactions between transcription factors. However, it is unclear how temporal-or organ-specific differences in epidermal patterning are achieved. Here we identify TRICHOMELESS1 (TCL1) as a new and major single-repeat MYBtype transcription factor that negatively regulates trichome formation in the inflorescence epidermis. A dominant mutant with elevated expression of TCL1 has a glabrous (trichomeless) phenotype, whereas a loss-of-function mutation in TCL1 uniquely confers ectopic trichome formation on inflorescence stem and pedicels. Genetic analyses demonstrate that TCL1 and CAPRICE work synergistically to regulate trichome patterning on these organs. Interestingly, overexpression of TCL1 specifically suppresses the expression of GLABRA1 (GL1), a crucial component in the trichome initiation complex, whereas loss-of-function of TCL1 enhances GL1 expression. Chromatin immunoprecipitation results show that TCL1 can be recruited to the cis-acting regulatory elements of GL1. These results provide the first molecular and genetic evidence that an R3 MYB may negatively regulate trichome cell specification in a novel manner by directly suppressing the transcription of GL1.
The position-dependent specification of root epidermal cells in Arabidopsis provides an elegant paradigm for cell patterning during development. Here, we describe a new gene, SCRAMBLED (SCM), required for cells to appropriately interpret their location within the developing root epidermis. SCM encodes a receptor-like kinase protein with a predicted extracellular domain of six leucine-rich repeats and an intracellular serine-threonine kinase domain. SCM regulates the expression of the GLABRA2, CAPRICE, WEREWOLF, and ENHANCER OF GLABRA3 transcription factor genes that define the cell fates. Further, the SCM gene is expressed throughout the developing root. Therefore, SCM likely enables developing epidermal cells to detect positional cues and establish an appropriate cell-type pattern.
Cell-type patterning in the Arabidopsis root epidermis is achieved by a network of transcription factors and influenced by a position-dependent mechanism. The SCRAMBLED receptor-like kinase is required for the normal pattern to arise, but its precise role is not understood. Here we describe genetic and molecular studies to define the spatial and temporal role of SCM in epidermal patterning and its relationship to the transcriptional network. Our results suggest that SCM helps unspecified epidermal cells interpret their position in relation to the underlying cortical cells and establish distinct cell identities. Furthermore, SCM loss-of-function and overexpression analyses suggest that SCM influences cell fate through its negative transcriptional regulation of the WEREWOLF MYB gene in epidermal cells at the H position. We also find that SCM function is specifically required for patterning the post-embryonic root epidermis and not for the analogous epidermal cell-type patterning during embryogenesis or hypocotyl development. In addition, we show that two closely related SCM-like genes in Arabidopsis (SRF1 and SRF3) are not required alone or together with SCM for proper epidermal patterning. These findings help define the developmental and mechanistic role of SCM and suggest a new model for its action in root epidermal cell patterning.
A fundamental aspect of multicellular development is the patterning of distinct cell types in appropriate locations. In this review, the molecular genetic control of cell-type pattern formation in the root epidermis of Arabidopsis thaliana is summarized. This developmental system represents a simple and genetically tractable example of plant cell patterning. The distribution of the two epidermal cell types, root-hair cells and non-hair cells, are generated by a combination of positional signalling and lateral inhibition mechanisms. In addition, recent evidence suggests that reinforcing mechanisms are used to ensure that the initial cell fate choice is adopted in a robust manner.
SCRAMBLED (SCM), a leucine-rich repeat receptor-like kinase, mediates positional signaling and cell-type pattern formation in the epidermis of Arabidopsis roots. The precise mechanism of SCM action has been unclear. In a recent report, we find that accumulation of the SCM-GFP fusion protein varies in a cell-type-specific manner during root epidermis development. At early stages, SCM-GFP accumulates equally in both root-hair cells and nonhair cells, but at later stages of epidermis development, it accumulates preferentially in root-hair cells. The importance of epidermal production of SCM was demonstrated by epidermis-specific SCM-GFP silencing, which caused an epidermal patterning defect. Further, the expression of SCM-GFP by a root-hair-cell promoter complements the scm-2 epidermal defect completely, whereas a non-hair-cell promoter complements the scm-2 epidermal phenotype partially. From these results we conclude that the spatial distribution of a positional cue and the accumulation of the SCM receptor are both required for optimal positional signaling in epidermal patterning.
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