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Molecular Profiling of Stomatal Meristemoids Reveals New Component of Asymmetric Cell Division and Commonalities among Stem Cell Populations in Arabidopsis

Department of Biology, University of Washington, Seattle, Washington 98195, USA.
The Plant Cell (Impact Factor: 9.58). 09/2011; 23(9):3260-75. DOI: 10.1105/tpc.111.088583
Source: PubMed

ABSTRACT The balance between maintenance and differentiation of stem cells is a central question in developmental biology. Development of stomata in Arabidopsis thaliana begins with de novo asymmetric divisions producing meristemoids, proliferating precursor cells with stem cell-like properties. The transient and asynchronous nature of the meristemoid has made it difficult to study its molecular characteristics. Synthetic combination of stomatal differentiation mutants due to loss- or gain-of-function mutations in SPEECHLESS, MUTE, and SCREAM create seedlings with an epidermis overwhelmingly composed of pavement cells, meristemoids, or stomata, respectively. Through transcriptome analysis, we define and characterize the molecular signatures of meristemoids. The reporter localization studies of meristemoid-enriched proteins reveals pathways not previously associated with stomatal development. We identified a novel protein, POLAR, and demonstrate through time-lapse live imaging that it exhibits transient polar localization and segregates unevenly during meristemoid asymmetric divisions. The polar localization of POLAR requires BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE. Comparative bioinformatic analysis of the transcriptional profiles of a meristemoid with shoot and root apical meristems highlighted cytokinin signaling and the ERECTA family receptor-like kinases in the broad regulation of stem cell populations. Our work reveals molecular constituents of stomatal stem cells and illuminates a common theme among stem cell populations in plants.

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Available from: Keiko U Torii, Jul 29, 2015
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    • "In these cells, BASL and POLAR proteins mark restricted areas of the cell periphery before division, indicating that these cells have the intrinsic ability to move components to regions that would be differentially inherited. Paradoxically, however, although analysis of BASL and POLAR revealed this polarization capacity, neither BASL nor POLAR is truly differentially segregated: a nuclear pool of BASL is inherited by both daughters (Dong et al., 2009) and POLAR is enriched but not exclusively present on one side of the cell (Pillitteri et al., 2011). In both cases, it is the post-divisional behaviours of the proteins that show clear differences between sisters. "
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    • "Thus division polarity is important for the regulation of cell fate determination, proliferation, and patterning during stomatal development. The BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) and POLAR proteins are novel proteins regulating stomatal divisions (Dong et al., 2009; Pillitteri et al., 2011 "
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    ABSTRACT: Stomata are two-celled valves that control epidermal pores whose opening and spacing optimizes shoot-atmosphere gas exchange. Arabidopsis stomatal formation involves at least one asymmetric division and one symmetric division. Stomatal formation and patterning are regulated by the frequency and placement of asymmetric divisions. This model system has already led to significant advances in developmental biology, such as the regulation of cell fate, division, differentiation, and patterning. Over the last 30 years, stomatal development has been found to be controlled by numerous intrinsic genetic and environmental factors. This mini review focuses on the signaling involved in stomatal initiation and in divisions in the cell lineage.
    Frontiers in Plant Science 06/2014; 5:297. DOI:10.3389/fpls.2014.00297 · 3.95 Impact Factor
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    • "In these cells, BASL and POLAR proteins mark restricted areas of the cell periphery before division, indicating that these cells have the intrinsic ability to move components to regions that would be differentially inherited. Paradoxically, however, although analysis of BASL and POLAR revealed this polarization capacity, neither BASL nor POLAR is truly differentially segregated: a nuclear pool of BASL is inherited by both daughters (Dong et al., 2009) and POLAR is enriched but not exclusively present on one side of the cell (Pillitteri et al., 2011). In both cases, it is the post-divisional behaviours of the proteins that show clear differences between sisters. "
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    ABSTRACT: Asymmetric cell divisions are formative divisions that generate daughter cells of distinct identity. These divisions are coordinated by either extrinsic ('niche-controlled') or intrinsic regulatory mechanisms and are fundamentally important in plant development. This review describes how asymmetric cell divisions are regulated during development and in different cell types in both the root and the shoot of plants. It further highlights ways in which omics and modelling approaches have been used to elucidate these regulatory mechanisms. For example, the regulation of embryonic asymmetric divisions is described, including the first divisions of the zygote, formative vascular divisions and divisions that give rise to the root stem cell niche. Asymmetric divisions of the root cortex endodermis initial, pericycle cells that give rise to the lateral root primordium, procambium, cambium and stomatal cells are also discussed. Finally, a perspective is provided regarding the role of other hormones or regulatory molecules in asymmetric divisions, the presence of segregated determinants and the usefulness of modelling approaches in understanding network dynamics within these very special cells. Asymmetric cell divisions define plant development. High-throughput genomic and modelling approaches can elucidate their regulation, which in turn could enable the engineering of plant traits such as stomatal density, lateral root development and wood formation.
    Annals of Botany 05/2014; 113(7). DOI:10.1093/aob/mcu065 · 3.30 Impact Factor
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