Cell cycle regulates cell type in the Arabidopsis sepal

Development (Impact Factor: 6.46). 10/2012; 139(23). DOI: 10.1242/dev.082925
Source: PubMed


The formation of cellular patterns during development requires the coordination of cell division with cell identity specification. This coordination is essential in patterning the highly elongated giant cells, which are interspersed between small cells, in the outer epidermis of the Arabidopsis thaliana sepal. Giant cells undergo endocycles, replicating their DNA without dividing, whereas small cells divide mitotically. We show that distinct enhancers are expressed in giant cells and small cells, indicating that these cell types have different identities as well as different sizes. We find that members of the epidermal specification pathway, DEFECTIVE KERNEL1 (DEK1), MERISTEM LAYER1 (ATML1), Arabidopsis CRINKLY4 (ACR4) and HOMEODOMAIN GLABROUS11 (HDG11), control the identity of giant cells. Giant cell identity is established upstream of cell cycle regulation. Conversely, endoreduplication represses small cell identity. These results show not only that cell type affects cell cycle regulation, but also that changes in the cell cycle can regulate cell type.

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    • "DEK1 is essential for seed, embryo, epidermis, trichome and SAM development, and subsequent plant growth. This unique plant calpain is also linked to syncytial nuclear divisions prior to the cellularization of several cell types, including aleurone and giant sepal cells (Brown et al. 1994, Roeder et al. 2012), yet little is known about how DEK1 acts at the cellular and molecular levels. The altered expression of the initial asymmetric zygotic division marker WOX2, the epidermal marker ATML1, the SAM-promoting genes WUS and STM, and the auxin transporter gene PIN4 presented here demonstrates a fundamental role for DEK1 during development. "
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    ABSTRACT: Eukaryotic development and stem cell control depend on the integration of cell positional sensing with cell cycle control and cell wall positioning, yet few factors that directly link these events are known. The DEFECTIVE KERNEL1 (DEK1) gene encoding the unique plant calpain protein is fundamental for development and growth, being essential to confer and maintain epidermal cell identity that allows development beyond the globular embryo stage. We show that DEK1 expression is highest in the actively dividing cells of seeds, meristems and vasculature. We further show that eliminating Arabidopsis DEK1 function leads to changes in developmental cues from the first zygotic division onward, altered microtubule patterns and misshaped cells resulting in early embryo abortion. Expression of the embryonic marker genes WOX2, ATML1, PIN4, WUS, and STM, related to axis organization, cell identity and meristem functions, are also altered in dek1 embryos. By monitoring cell layer-specific DEK1 down-regulation, we show that L1- and 35S-induced down-regulation mainly affects stem cell functions, causing severe shoot apical meristem phenotypes. These results are consistent with a requirement for DEK1 to direct layer-specific cellular activities and set downstream developmental cues. Our data suggest that DEK1 may anchor cell wall positions and control cell division and differentiation, thereby balancing the plant's requirement to maintain totipotent stem cell reservoirs while simultaneously directing growth and organ formation. A role for DEK1 in regulating microtubule-orchestrated cell wall orientation during cell division can explain its effects on embryonic development, and suggests a more general function for calpains in microtubule organization in eukaryotic cells. © The Author 2015. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For Permissions, please e-mail:
    Plant and Cell Physiology 07/2015; 56(9). DOI:10.1093/pcp/pcv110 · 4.93 Impact Factor
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    • "Apoplastic signalling mediated by ACR4, like DEK1 function, is necessary for the maintenance of HD-ZIP IV gene expression (San-Bento et al., 2014). However, genetic analysis carried out in Arabidopsis and maize (Becraft et al., 2002; Roeder et al., 2012) suggests that DEK1 and ACR4 act in parallel. "
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    ABSTRACT: During plant epidermal development, many cell types are generated from protodermal cells, a process requiring complex coordination of cell division, growth, endoreduplication and the acquisition of differentiated cellular morphologies. Here we show that the Arabidopsis phytocalpain DEFECTIVE KERNEL 1 (DEK1) promotes the differentiated epidermal state. Plants with reduced DEK1 activity produce cotyledon epidermis with protodermal characteristics, despite showing normal growth and endoreduplication. Furthermore, in non-embryonic tissues (true leaves, sepals), DEK1 is required for epidermis differentiation maintenance. We show that the HD-ZIP IV family of epidermis-specific differentiation-promoting transcription factors are key, albeit indirect, targets of DEK1 activity. We propose a model in which DEK1 influences HD-ZIP IV gene expression, and thus epidermis differentiation, by promoting cell adhesion and communication in the epidermis.
    Development 05/2015; DOI:10.1242/dev.122325 · 6.46 Impact Factor
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    • "RESEARCH ARTICLE Development (2015) 142, 1-11 doi:10.1242/dev.117168 DEVELOPMENT (Roeder et al., 2012). The HDG1-mediated increase in cell ploidy in leaves might be a secondary consequence of the increase in margin cells. "
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    ABSTRACT: AINTEGUMENTA-LIKE (AIL) transcription factors are key regulators of cell proliferation and meristem identity. Although AIL functions have been well described, the direct signalling components of this pathway are largely unknown. We show that BABY BOOM (BBM) and other AIL proteins physically interact with multiple members of the L1-expressed HOMEODOMAIN GLABROUS (HDG) transcription factor family, including HDG1, HDG11 and HDG12. Overexpression of HDG1, HDG11 and HDG12 restricts growth due to root and shoot meristem arrest, which is associated with reduced expression of genes involved in meristem development and cell proliferation pathways, whereas downregulation of multiple HDG genes promotes cell overproliferation. These results suggest a role for HDG proteins in promoting cell differentiation. We also reveal a transcriptional network in which BBM and HDG1 regulate several common target genes, and where BBM/AIL and HDG regulate the expression of each other. Taken together, these results suggest opposite roles for AIL and HDG proteins, with AILs promoting cell proliferation and HDGs stimulating cell differentiation, and that these functions are mediated at both the protein-protein interaction and transcriptional level. © 2015. Published by The Company of Biologists Ltd.
    Development 01/2015; 142(3). DOI:10.1242/dev.117168 · 6.46 Impact Factor
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