The Recessive Epigenetic swellmap Mutation Affects the Expression of Two Step II Splicing Factors Required for the Transcription of the Cell Proliferation Gene STRUWWELPETER and for the Timing of Cell Cycle Arrest in the Arabidopsis Leaf

Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Conecticut 06520-8104, USA.
The Plant Cell (Impact Factor: 9.34). 08/2005; 17(7):1994-2008. DOI: 10.1105/tpc.105.032771
Source: PubMed


Generally, cell division can be uncoupled from multicellular development, but more recent evidence suggests that cell cycle progression and arrest is coupled to organogenesis and growth. We describe a recessive mutant, swellmap (smp), with reduced organ size and cell number. This defect is partially compensated for by an increase in final cell size. The mutation causes a precocious arrest of cell proliferation in the organ primordium and possibly reduces the rate of cell division there. The mutation proved to be an epigenetic mutation (renamed smp(epi)) that defined a single locus, SMP1, but affected the expression of both SMP1 and a second very similar gene, SMP2. Both genes encode CCHC zinc finger proteins with similarities to step II splicing factors involved in 3' splice site selection. Genetic knockouts demonstrate that the genes are functionally redundant and essential. SMP1 expression is associated with regions of cell proliferation. Overexpression of SMP1 produced an increase in organ cell number and a partial decrease in cell expansion. The smp(epi) mutation does not affect expression of eukaryotic cell cycle regulator genes CYCD3;1 and CDC2A but affects expression of the cell proliferation gene STRUWWELPETER (SWP) whose protein has similarities to Med150/Rgr1-like subunits of the Mediator complex required for transcriptional activation. Introduction of SWP cDNA into smp(epi) plants fully restored them to wild-type, but the expression of both SMP1 and SMP2 were also restored in these lines, suggesting a physical interaction among the three proteins and/or genes. We propose that step II splicing factors and a transcriptional Mediator-like complex are involved in the timing of cell cycle arrest during leaf development.

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    • "A number of lines of evidence do indeed indicate that altered cell division pattern does influence leaf shape. For example, mutants in which leaf morphology is altered often display an altered pattern of division termination (Nath et al., 2003), and an extended phase of cell proliferation has frequently been associated with alterations in leaf size and shape (Mizukami and Fischer, 2000; Autran et al., 2002; Clay and Nelson, 2005). Furthermore, experiments in which genes encoding components of the cell cycle have been misexpressed have often led to altered leaf morphology. "
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    ABSTRACT: Understanding the relationship of the size and shape of an organism to the size, shape, and number of its constituent cells is a basic problem in biology; however, numerous studies indicate that the relationship is complex and often nonintuitive. To investigate this problem, we used a system for the inducible expression of genes involved in the G1/S transition of the plant cell cycle and analyzed the outcome on leaf shape. By combining a careful developmental staging with a quantitative analysis of the temporal and spatial response of cell division pattern and leaf shape to these manipulations, we found that changes in cell division frequency occurred much later than the observed changes in leaf shape. These data indicate that altered cell division frequency cannot be causally involved in the observed change of shape. Rather, a shift to a smaller cell size as a result of the genetic manipulations performed correlated with the formation of a smoother leaf perimeter, i.e. appeared to be the primary cellular driver influencing form. These data are discussed in the context of the relationship of cell division, growth, and leaf size and shape.
    Plant physiology 06/2011; 156(4):2196-206. DOI:10.1104/pp.111.176073 · 6.84 Impact Factor
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    • "Ectopic expression of these genes in Arabidopsis prolongs the duration of cell proliferation, leading to the production of larger organs with more cells, while mutations in the genes encoding these factors reduce the duration of cell proliferation and thus result in smaller organs (Mizukami & Fischer, 2000; Autran et al., 2002; Dinneny et al., 2004; Ohno et al., 2004; Clay & Nelson, 2005; Horiguchi et al., 2005; Anastasiou et al., 2007; Lee et al., 2009). By contrast, some other factors, including AUXIN RESPONSE FACTOR2 (ARF2), BLADE ON PETIOLE1 (BOP1), PEAPOD1 ⁄ 2 (PPDs), BIG BROTHER (BB) and DA1, appear to restrict organ growth by limiting the period of proliferation, because loss of function in each of these genes results in enlarged organs as a result of the increased cell number (Ha et al., 2003; Disch et al., 2006; Schruff et al., 2006; White, 2006; Li et al., 2008). "
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    ABSTRACT: • The growth of a plant organ to its characteristic size is regulated by an elaborate developmental program involving both internal and external signals. Here, we identify a novel Arabidopsis gene, ORGAN SIZE RELATED1 (OSR1), that is involved in regulation of organ growth and overall organ size. • A combination of genetic, cytological and molecular approaches was used to characterize the expression profile, subcellular localization and roles of OSR1 during organ growth. • Ectopic expression of OSR1 in Arabidopsis resulted in enlarged organs, as a consequence of increases in both cell number and cell size. OSR1 shares a conserved OSR domain with ARGOS and ARGOS-LIKE (ARL), which is sufficient for their functions in promoting organ growth. OSR1 is a plant hormone-responsive gene and appears to act redundantly with ARGOS and ARL during organ growth. The OSR proteins are localized to the endoplasmic reticulum. • Our results suggest that three co-evolved members of the OSR family may act coordinately to orchestrate growth signals and cell proliferation and expansion, thereby affecting organ growth and final organ size.
    New Phytologist 04/2011; 191(3):635-46. DOI:10.1111/j.1469-8137.2011.03710.x · 7.67 Impact Factor
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    • "For example, the loss-of-function mutation in the AN3/ GRF-INTERACTING FACTOR1 gene (Kim and Kende, 2004), which positively regulates cell proliferation in leaf primordia, causes the typical compensation syndrome (Horiguchi et al., 2005). Similarly, several other mutations that affect leaf cell proliferation have been described to cause the compensation syndrome, including aintegumenta (ant), struwwelpeter, swellmap, G-protein a-subunit1 (gpa1), and deformed roots and leaves1 (Mizukami and Fischer, 2000; Ullah et al., 2001; Autran et al., 2002; Nelissen et al., 2003; Clay and Nelson, 2005). Impaired cell proliferation caused by the reduced activity of cyclin-dependent kinases also induces compensation in leaves (Hemerly et al., 1995; Wang et al., 2000; De Veylder et al., 2001; Boudolf et al., 2004). "
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    ABSTRACT: In multicellular organisms, the coordination of cell proliferation and expansion is fundamental for proper organogenesis, yet the molecular mechanisms involved in this coordination are largely unexplored. In plant leaves, the existence of this coordination is suggested by compensation, in which a decrease in cell number triggers an increase in mature cell size. To elucidate the mechanisms of compensation, we isolated five new Arabidopsis (Arabidopsis thaliana) mutants (fugu1-fugu5) that exhibit compensation. These mutants were characterized together with angustifolia3 (an3), erecta (er), and a KIP-RELATED PROTEIN2 (KRP2) overexpressor, which were previously reported to exhibit compensation. Time-course analyses of leaf development revealed that enhanced cell expansion in fugu2-1, fugu5-1, an3-4, and er-102 mutants is induced postmitotically, indicating that cell enlargement is not caused by the uncoupling of cell division from cell growth. In each of the mutants, either the rate or duration of cell expansion was selectively enhanced. In contrast, we found that enhanced cell expansion in KRP2 overexpressor occurs during cell proliferation. We further demonstrated that enhanced cell expansion occurs in cotyledons with dynamics similar to that in leaves. In contrast, cell expansion was not enhanced in roots even though they exhibit decreased cell numbers. Thus, compensation was confirmed to occur preferentially in determinate organs. Flow cytometric analyses revealed that increases in ploidy level are not always required to trigger compensation, suggesting that compensation is only partially mediated by ploidy-dependent processes. Our results suggest that compensation reflects an organ-wide coordination of cell proliferation and expansion in determinate organs, and involves at least three different expansion pathways.
    Plant physiology 07/2007; 144(2):988-99. DOI:10.1104/pp.107.099325 · 6.84 Impact Factor
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