Stomatal development: A plant's perspective on cell polarity, cell fate transitions and intercellular communication

Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305-5020, USA.
Development (Impact Factor: 6.27). 10/2012; 139(20):3683-92. DOI: 10.1242/dev.080523
Source: PubMed

ABSTRACT The plant stomatal lineage manifests features common to many developmental contexts: precursor cells are chosen from an initially equivalent field of cells, undergo asymmetric and self-renewing divisions, communicate among themselves and respond to information from a distance. As we review here, the experimental accessibility of these epidermal lineages, particularly in Arabidopsis, has made stomata a conceptual and technical framework for the study of cell fate, stem cells, and cell polarity in plants.

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    • "The localization and levels of BASL and SPCH have been tracked in developing leaves which led to a " polarity switching " model that predicts the sitting of the BASL protein during successive divisions (Robinson et al., 2011). The regulation of asymmetric divisions during stomatal development has been comprehensively discussed in recent reviews (Lau and Bergmann, 2012; Pillitteri and Torii, 2012; Wengier and Bergmann, 2012). Here we emphasize recent work on the control of terminal divisions in stomatal development. "
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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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    • "Three basic-helix–loop–helix (bHLH) transcription factors, SPEECHLESS (SPCH), MUTE, and FAMA, are required for the successive stages of stomatal development (Ohashi- Ito and Bergmann, 2006; MacAlister et al., 2007; Pillitteri et al., 2007). SPCH is essential for MMC formation, stomatal entry divisions, and maintenance of meristemoid stem cell activity (Pillitteri and Torii, 2012; Lau and Bergmann, 2012). MUTE promotes the transition of meristemoids into GMCs (Pillitteri et al., 2007). "
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    ABSTRACT: The Arabidopsis stoma is a specialized epidermal valve made up of a pair of guard cells around a pore whose aperture controls gas exchange between the shoot and atmosphere. Guard cells (GCs) are produced by a symmetric division of guard mother cells (GMCs). The R2R3-MYB transcription factor FOUR LIPS (FLP) and its paralogue MYB88 restrict the division of a GMC to one. Previously, the upstream regions of several core cell cycle genes were identified as the direct targets of FLP/MYB88, including the B-type cyclin-dependent kinase CDKB1;1 and A2-type cyclin CYCA2;3. Here we show that CDKA;1 is also an immediate direct target of FLP/MYB88 through the binding to cis-regulatory elements in the CDKA;1 promoter region. CDKA;1 activity is required not only for normal GMC divisions but also for the excessive cell overproliferation in flp myb88 mutant GMCs. The impaired defects of GMC division in cdkb1;1 1;2 mutants could be partially rescued by a stage-specific expression of CDKA;1. Although targeted overexpression of CDKA;1 does not affect stomatal development, ectopic expression of the D3-type cyclin CYCD3;2 induces GC subdivision, resulting in a stoma with 3-4 GCs instead of the normal two. Co-overexpression of CDKA;1 with CYCD3;2, but not with CYCA2;3, confers a synergistic effect with respect to GC subdivision. Thus, in addition to a role in stomatal formative asymmetric divisions at early developmental stages, CDKA;1 is needed in triggering GMC symmetric divisions at the late stage of stomatal development. However, timely down-regulation of CDKA;1-CYCD3 activity is required for restriction of GC proliferation.
    Journal of Experimental Botany 03/2014; 65(9). DOI:10.1093/jxb/eru139 · 5.79 Impact Factor
    • "There are many known density and patterning mutants (e.g. fama, spch, mute, and tmm) in which specific gene mutations have resulted in changes to cell division and differentiation and altered patterns of stomata and epidermal cells, resulting in stomatal pairing or clustering in which the " one-cell-spacing " rule is broken (for review, see Lau and Bergmann, 2012). The one-cell-spacing rule refers to the fact that stomata are separated from each other by a minimum of one cell, enabling efficient stomatal operation (Serna and Fenoll, 2000) and maintaining the efficiency of gas fluxes (Nadeau and Sack, 2002). "
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    ABSTRACT: The control of gaseous exchange between the leaf and bulk atmosphere by stomata governs photosynthetic CO2 uptake for photosynthesis and transpiration, determining plant productivity and water use efficiency. The balance between these two processes depends on stomatal responses to environmental and internal cues and the synchrony of stomatal behaviour relative to mesophyll demands for CO2. Here we examine the rapidity of stomatal responses with attention to their relationship to photosynthetic CO2 uptake, and the consequences for water use. We discuss the influence of anatomical characteristics on the velocity of changes in stomatal conductance, and explore the potential for manipulating the physical as well as physiological characteristics of stomatal guard cells in order to accelerate stomatal movements in synchrony with mesophyll CO2 demand, and to improve water use efficiency without substantial cost to photosynthetic carbon fixation. We conclude that manipulating guard cell transport and metabolism is just as, if not more likely to yield useful benefits as manipulations of their physical and anatomical characteristics. Achieving these benefits should be greatly facilitated by quantitative systems analysis that connects directly the molecular properties of the guard cells to their function in the field.
    Plant physiology 02/2014; 164(4). DOI:10.1104/pp.114.237107 · 7.39 Impact Factor
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