BASL Controls Asymmetric Cell Division in Arabidopsis

Dong, Juan; MacAlister, Cora A.; Bergmann, Dominique C.

doi:10.1016/j.cell.2009.04.018

Cited by 277 publications

(403 citation statements)

References 48 publications

(78 reference statements)

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“…All these genes have the ability to turn cell division into a deterministic process allowing the plant to develop stereotypical cellular patterns. However, the cells of basl, pan, and pol pll1 mutants appear to divide symmetrically (40)(41)(42). This result supports the idea that the mechanism we have outlined is the default division mechanism on which polar signals can act to create precise cellular patterns.…”

Section: Discussionsupporting

confidence: 77%

Universal rule for the symmetric division of plant cells

Besson

Dumais²

2011

Proc. Natl. Acad. Sci. U.S.A.

197

213

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The division of eukaryotic cells involves the assembly of complex cytoskeletal structures to exert the forces required for chromosome segregation and cytokinesis. In plants, empirical evidence suggests that tensional forces within the cytoskeleton cause cells to divide along the plane that minimizes the surface area of the cell plate (Errera's rule) while creating daughter cells of equal size. However, exceptions to Errera's rule cast doubt on whether a broadly applicable rule can be formulated for plant cell division. Here, we show that the selection of the plane of division involves a competition between alternative configurations whose geometries represent local area minima. We find that the probability of observing a particular division configuration increases inversely with its relative area according to an exponential probability distribution known as the Gibbs measure. Moreover, a comparison across land plants and their most recent algal ancestors confirms that the probability distribution is widely conserved and independent of cell shape and size. Using a maximum entropy formulation, we show that this empirical division rule is predicted by the dynamics of the tense cytoskeletal elements that lead to the positioning of the preprophase band. Based on the fact that the division plane is selected from the sole interaction of the cytoskeleton with cell shape, we posit that the new rule represents the default mechanism for plant cell division when internal or external cues are absent.plant development | mitosis | tissue morphogenesis

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Section: Discussionsupporting

confidence: 77%

Universal rule for the symmetric division of plant cells

Besson

Dumais²

2011

Proc. Natl. Acad. Sci. U.S.A.

197

213

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“…At present, we cannot distinguish if loss of RBR function increases the number of cells entering the stomatal lineage or results in proliferation of protodermal cells or MMCs, which are not yet committed to guard cell morphogenesis. The failure to undergo asymmetric divisions alone is unlikely the cause for this lack of commitment because cells in the breaking of asymmetry in the stomatal lineage1 mutant that are produced by incorrect symmetric divisions express MUTE and can form normal stomates (Dong et al, 2009). It is possible, therefore, that the TMM-expressing cells in the RBRi leaf represent protodermal or postprotodermal cells, in which restrictive signaling through TMM/ER/EPF2 cannot arrest cell cycle activity in the absence of RBR.…”

Section: Rbr Promotes Entry Into Cell Differentiationmentioning

confidence: 99%

ArabidopsisRETINOBLASTOMA-RELATED Is Required for Stem Cell Maintenance, Cell Differentiation, and Lateral Organ Production

et al. 2010

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Several genes involved in the regulation of postembryonic organ initiation and growth have been identified. However, it remains largely unclear how developmental cues connect to the cell cycle. RETINOBLASTOMA RELATED (RBR) is a plant homolog of the tumor suppressor Retinoblastoma (pRb), which is a key regulator of the cell cycle. Using inducible RNA interference (RNAi) against Arabidopsis thaliana RBR (RBRi), we reduced RBR expression levels at different stages of plant development. Conditional reduction or loss of RBR function disrupted cell division patterns, promoted context-dependent cell proliferation, and negatively influenced establishment of cell differentiation. Several lineages of toti-and pluripotent cells, including shoot apical meristem stem cells, meristemoid mother cells, and procambial cells, failed to produce appropriately differentiated cells. Meristem activity was altered, leading to a disruption of the CLAVATA-WUSCHEL feedback loop and inhibition of lateral organ formation. Release of RBR from RNAi downregulation restored meristem activity. Gene profiling analyses soon after RBRi induction revealed that a change in RBR homeostasis is perceived as a stress, even before genes regulated by RBR-E2F become deregulated. The results establish RBR as a key cell cycle regulator required for coordination of cell division, differentiation, and cell homeostasis. INTRODUCTIONRetinoblastoma (RB) was the first tumor suppressor gene identified in animals (Friend et al., 1986) and later was associated with cell cycle regulation, thus establishing pRb as a key regulator of cell proliferation. In animals, three members of the RB family of proteins (pRb, p107, and p130), also referred to as pocket proteins (Mulligan and Jacks, 1998), negatively regulate the G1-to-S phase transition during the cell cycle. It is now widely accepted that mitogenic signals activate several cyclin-dependent kinase (CDK)-cyclin complexes during progression through G1 to phosphorylate pRb, thereby releasing it from interactions with E2F/DP transcription factor complexes to facilitate S-phase entry (Weinberg, 1995). Subsequently, pRb was also found to regulate tissue-specific transcription factors that regulate cell differentiation, such as MyoD, which activates muscle-specific genes (De Falco et al., 2006). pRb also regulates germ cell proliferation, differentiation, and survival (Toppari et al., 2003) and is required for osteoblast, keratinocyte, and macrophage differentiation (Nead et al., 1998;Liu et al., 1999;Thomas et al., 2003). Together with the tumor suppressor p53, pRb regulates adipocyte differentiation and function (Hallenborg et al., 2009). The requirement for RB in cell differentiation therefore extends beyond regulation of cell cycle entry. For example, the loss of RB function in cardioblasts affects cell differentiation by modulating the activity of cardiogenic factors (Papadimou et al., 2005).RB-related genes, termed RETINOBLASTOMA-RELATED (RBR; Ach et al., 1997), are also found in monocots (Grafi et al., 1996;Xie et al...

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“…Such divisions are often physically asymmetric as well, producing daughters with distinct sizes and/or shapes. Many observations suggest mechanistic links between physical and developmental asymmetry (Gallagher and Smith, 2000;Song et al, 2008;Dong et al, 2009). Moreover, orientation of division polarity is crucial for proper placement of the daughter cells within developing tissues to create functional cellular arrangements.…”

Section: Introductionmentioning

confidence: 99%

“…Ligandreceptor interactions act through a mitogen-activated protein kinase signaling cascade to regulate the occurrence and orientation of stomate-forming asymmetric divisions (Pillitteri and Torii, 2012). BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) and POLAR LOCALIZATION DURING ASYMMETRIC DIVISION AND REDISTRIBUTION (POLAR) act downstream to promote division polarity (Dong et al, 2009;Pillitteri et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Identification of PAN2 by Quantitative Proteomics as a Leucine-Rich Repeat–Receptor-Like Kinase Acting Upstream of PAN1 to Polarize Cell Division in Maize

et al. 2012

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Mechanisms governing the polarization of plant cell division are poorly understood. Previously, we identified pangloss1 (PAN1) as a leucine-rich repeat-receptor-like kinase (LRR-RLK) that promotes the polarization of subsidiary mother cell (SMC) divisions toward the adjacent guard mother cell (GMC) during stomatal development in maize (Zea mays). Here, we identify pangloss2 (PAN2) as a second LRR-RLK promoting SMC polarization. Quantitative proteomic analysis identified a PAN2 candidate by its depletion from membranes of pan2 single and pan1;pan2 double mutants. Genetic mapping and sequencing of mutant alleles confirmed the identity of this protein as PAN2. Like PAN1, PAN2 has a catalytically inactive kinase domain and accumulates in SMCs at sites of GMC contact before nuclear polarization. The timing of polarized PAN1 and PAN2 localization is very similar, but PAN2 acts upstream because it is required for polarized accumulation of PAN1 but is independent of PAN1 for its own localization. We find no evidence that PAN2 recruits PAN1 to the GMC contact site via a direct or indirect physical interaction, but PAN2 interacts with itself. Together, these results place PAN2 at the top of a cascade of events promoting the polarization of SMC divisions, potentially functioning to perceive or amplify GMC-derived polarizing cues.

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BASL Controls Asymmetric Cell Division in Arabidopsis

Cited by 277 publications

References 48 publications

Universal rule for the symmetric division of plant cells

Universal rule for the symmetric division of plant cells

ArabidopsisRETINOBLASTOMA-RELATED Is Required for Stem Cell Maintenance, Cell Differentiation, and Lateral Organ Production

Identification of PAN2 by Quantitative Proteomics as a Leucine-Rich Repeat–Receptor-Like Kinase Acting Upstream of PAN1 to Polarize Cell Division in Maize

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