Termination of asymmetric cell division and differentiation of stomata. Nature

Department of Biology, University of Washington, Seattle, Washington 98195, USA.
Nature (Impact Factor: 41.46). 03/2007; 445(7127):501-5. DOI: 10.1038/nature05467
Source: PubMed


Stomata consist of a pair of guard cells that mediate gas and water-vapour exchange between plants and the atmosphere. Stomatal precursor cells-meristemoids-possess a transient stem-cell-like property and undergo several rounds of asymmetric divisions before further differentiation. Here we report that the Arabidopsis thaliana basic helix-loop-helix (bHLH) protein MUTE is a key switch for meristemoid fate transition. In the absence of MUTE, meristemoids abort after excessive asymmetric divisions and fail to differentiate stomata. Constitutive overexpression of MUTE directs the entire epidermis to adopt guard cell identity. MUTE has two paralogues: FAMA, a regulator of guard cell morphogenesis, and SPEECHLESS (SPCH). We show that SPCH directs the first asymmetric division that initiates stomatal lineage. Together, SPCH, MUTE and FAMA bHLH proteins control stomatal development at three consecutive steps: initiation, meristemoid differentiation and guard cell morphogenesis. Our findings highlight the roles of closely related bHLHs in cell type differentiation in plants and animals.

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Available from: Keiko U Torii, Jan 19, 2016
    • "A similar trend was observed for the EPF1 gene encoding a negative regulator of stomatal formation secreted by stomatal precursors, from late meristemoids to guard mother cells, as well as GCs (Hara et al., 2007) (Fig. 2C) and for two of three bHLH transcription factors genes, MUTE and FAMA (Fig. 2D). MUTE and FAMA are involved in the later stages of stomata formation, in the specification of GC precursors and their symmetric division (Pillitteri et al., 2007). In contrast, no changes were observed for transcription of SPEECHLESS bHLH transcription factor and EPF2 genes, both involved in the initial specification of the meristemoid in the stomatal lineage (Fig. 2C, D). "
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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:
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    • "Likewise, the 'master regulator' activities of SPCH and MUTE have made it appealing to consider them as segregated determinants, but the details of their expression patterns make this unlikely. When SPCH or MUTE expressing cells divide, both daughters inherit maternal proteins; it is differential maintenance of the proteins that distinguish the daughters (MacAlister et al., 2007; Pillitteri et al., 2007, 2008; Lampard et al., 2008; Robinson et al., 2011). Other examples of intrinsic control can be hypothesized based on available data. "

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    • "For example, the loss of TMM or YODA function results in the production of excess stomata in contact. Three basic helix-loop-helix (bHLH) transcription factors, SPEECHLESS (SPCH), MUTE, and FAMA, are required for successive stages of development including lineage initiation and proliferation, as well as terminal differentiation (Ohashi-Ito and Bergmann, 2006; MacAlister et al., 2007; Pillitteri et al., 2007). "
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    ABSTRACT: The initiation of stomatal lineage and subsequent asymmetric divisions in Arabidopsis require the activity of the basic helix-loop-helix transcription factor SPEECHLESS (SPCH). It has been shown that SPCH controls entry into the stomatal lineage as a substrate either of the MITOGEN-ACTIVATED PROTEIN KINASE (MAPK) cascade or GSK3-like kinase BRASSINOSTEROID INSENSITIVE 2 (BIN2). Here we show that three serine residues of SPCH appear to be the primary phosphorylation targets of Cyclin-Dependent Kinases A;1 (CDKA;1) in vitro, and among them Serine 186 plays a crucial role in stomatal formation. Expression of an SPCH construct harboring a mutation that results in phosphorylation deficiencies on Serine 186 residue failed to rescue stomatal defects in spch null mutants. Expression of a phosphorylation-mimic mutant SPCH(S186D) complemented stomatal production defects in the transgenic lines harboring the targeted expression of dominant-negative CDKA;1.N146. Therefore, in addition to MAPK- and BIN2-mediated phosphorylation on SPCH, phosphorylation at Serine 186 is positively required for SPCH function in regulating stomatal development. Copyright © 2015 The Author. Published by Elsevier Inc. All rights reserved.
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