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: 9.34). 09/2011; 23(9):3260-75. DOI: 10.1105/tpc.111.088583
Source: PubMed


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, Oct 07, 2015
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    • "ne JA - Ile is known to be involved in the repression of cell proliferation and cell size during leaf growth ( Noir et al . , 2013 ) , the relation of JA - Ile to PPD function is currently unclear . Interestingly , JAZ10 was also found to be upregulated in the meristemoid - enriched scrm - D ; mute mutant and is expressed in the stomatal lineage ( Pillitteri et al . , 2011 ) . KIX8 and KIX9 were also identified in Arabidopsis TIFY8 protein complexes and TIFY8 heterodimerized with PPD1 and PPD2 , but not with any JAZ protein ( Cuéllar Pérez et al . , 2014 ) . Although a TIFY8 ortholog can be found in the moss Physcomitrella patens , hinting at a more ancient evolutionary origin compared with PPD1 / 2 and K"
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    ABSTRACT: Cell number is an important determinant of final organ size. In the leaf, a large proportion of cells are derived from the stomatal lineage. Meristemoids, which are stem cell-like precursor cells, undergo asymmetric divisions, generating several pavement cells adjacent to the two guard cells. However, the mechanism controlling the asymmetric divisions of these stem cells prior to differentiation is not well understood. Here, we characterized PEAPOD (PPD) proteins, the only transcriptional regulators known to negatively regulate meristemoid division. PPD proteins interact with KIX8 and KIX9, which act as adaptor proteins for the corepressor TOPLESS. D3-type cyclin encoding genes were identified among direct targets of PPD2, being negatively regulated by PPDs and KIX8/9. Accordingly, kix8 kix9 mutants phenocopied PPD loss-of-function producing larger leaves resulting from increased meristemoid amplifying divisions. The identified conserved complex might be specific for leaf growth in the second dimension, since it is not present in Poaceae (grasses), which also lack the developmental program it controls. © 2015 American Society of Plant Biologists. All rights reserved.
    The Plant Cell 07/2015; 27(8). DOI:10.1105/tpc.15.00006 · 9.34 Impact Factor
    • "The regulation of stomatal development also involves the mitogen-activated protein kinases cascade signal transduction chain (Bergmann et al., 2004; Shpak et al., 2005) and the action of the basic helix–loop–helix (bHLH) transcription factors SPEECHLESS, MUTE, and FAMA (Pillitteri and Torii, 2007), and SCREAM (SCRM) and SCRM2, which interact directly with and specify the consecutive action of the above-mentioned bHLH factors (Kanaoka et al., 2008). In addition, protein factors that regulate asymmetric (Bergmann et al., 2009; Dong et al., 2009; Pillitteri et al., 2011) and symmetric cell division, e.g. FLP and MYB88 factors (Yang and Sack, 1995; Lee et al., 2013, 2014) are key to executing the controlled morphogenesis of stomata. "
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    ABSTRACT: The initiation of stomata, microscopic valves in the epidermis of higher plants that control of gas exchange, requires a co-ordinated sequence of asymmetric and symmetric divisions, which is under tight environmental and developmental control. Arabidopsis leaves grown under elevated photosynthetic photon flux density have a higher density of stomata. STOMAGEN encodes an epidermal patterning factor produced in the mesophyll, and our observations indicated that elevated photosynthetic irradiation stimulates STOMAGEN expression. Our analysis of gain and loss of function of STOMAGEN further detailed its function as a positive regulator of stomatal formation on both sides of the leaf, not only in terms of stomatal density across the leaf surface but also in terms of their stomatal index. STOMAGEN function was rate limiting for the light response of the stomatal lineage in the adaxial epidermis. Mutants in pathways that regulate stomatal spacing in the epidermis and have elevated stomatal density, such as stomatal density and distribution (sdd1) and too many mouth alleles, displayed elevated STOMAGEN expression, suggesting that STOMAGEN is either under the direct control of these pathways or is indirectly affected by stomatal patterning, suggestive of a feedback mechanism. These observations support a model in which changes in levels of light irradiation are perceived in the mesophyll and control the production of stomata in the epidermis by mesophyll-produced STOMAGEN, and whereby, conversely, stomatal patterning, either directly or indirectly, influences STOMAGEN levels. © The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email:
    Journal of Experimental Botany 05/2015; 66(15). DOI:10.1093/jxb/erv233 · 5.53 Impact Factor
    • "Intrinsic mechanisms in plant ACD have been elusive, in part, because of the lack of homologs of the conserved regulators in animals. The recent discovery of the plant polarity proteins BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) (Dong et al., 2009) and POLAR (Pillitteri et al., 2011) revealed that intrinsic elements, behaving similarly to the conserved Par proteins in animals, control stem cell ACD in Arabidopsis. BASL is required for the development and patterning of stomata—breathing pores in plant epidermis. "
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    ABSTRACT: Cell polarization is linked to fate determination during asymmetric division of plant stem cells, but the underlying molecular mechanisms remain unknown. In Arabidopsis, BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) is polarized to control stomatal asymmetric division. A mitogen-activated protein kinase (MAPK) cascade determines terminal stomatal fate by promoting the degradation of the lineage determinant SPEECHLESS (SPCH). Here, we demonstrate that a positive-feedback loop between BASL and the MAPK pathway constitutes a polarity module at the cortex. Cortical localization of BASL requires phosphorylation mediated by MPK3/6. Phosphorylated BASL functions as a scaffold and recruits the MAPKKK YODA and MPK3/6 to spatially concentrate signaling at the cortex. Activated MPK3/6 reinforces the feedback loop by phosphorylating BASL and inhibits stomatal fate by phosphorylating SPCH. Polarization of the BASL-MAPK signaling feedback module represents a mechanism connecting cell polarity to fate differentiation during asymmetric stem cell division in plants. Copyright © 2015 Elsevier Inc. All rights reserved.
    Developmental Cell 04/2015; DOI:10.1016/j.devcel.2015.02.022 · 9.71 Impact Factor
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