Nuclear envelope radiating microtubules in plant cells during interphase mitosis transition

Bakhuizen, R.; Spronsen, Paulina C. van; Hertog, F. A. J. Sluiman-den; Venverloo, Catharina J.; Roo, Leentje Goosen‐De

doi:10.1007/bf01273234

Cited by 55 publications

(23 citation statements)

References 20 publications

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“…Experimental observations indicate that the distribution of strands, or more specifically their associated microtubules, anticipates the position of the PPB; that is, the PPB typically forms on the walls that receive the most endoplasmic microtubules (18,19,25) (Fig. 5 C and D).…”

Section: Resultsmentioning

confidence: 99%

“…Given the central role played by the PPB in guiding the cell plate, events leading to its positioning are of particular interest for understanding the selection of the division plane. Observations of premitotic cells have established that cytoplasmic strands populated by microtubules and actin filaments span the space between the nucleus and the cell surface (18)(19)(20)(21). Laser-ablation experiments demonstrate that these strands are under tension (22,23) and are likely responsible for maintaining the nucleus in a central position.…”

mentioning

confidence: 99%

“…The tensional forces would also explain the tendency of the strands to span the shortest distance between the nucleus and the cell surface (21,24). During preprophase, these strands stabilize cortical microtubules recruited for the PPB and ultimately coalesce into a cytoskeletal structure known as the phragmosome that bridges the nucleus and the cell cortex (18,19). Because the phragmosome is made of tensile cytoskeletal elements, it naturally converges to a plane of least area.…”

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confidence: 99%

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Universal rule for the symmetric division of plant cells

Besson

Dumais²

2011

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

192

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: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Universal rule for the symmetric division of plant cells

Besson

Dumais²

2011

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

192

213

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“…In root cells of the male fern Dryopteris filix-mas where the nucleus is close to the plasma membrane, electron microscopy images suggest that cytoplasmic microtubules connected to the nucleus could bend when reaching the cortex and be intermingled with PPB microtubules (33). Based on these observations, but without further experimental proof, microtubules populating cytoplasmic strands were also proposed to bend and interact with PPB microtubules (34). Light-transmitted microscopic observations of vacuolated cells also attested to the close vicinity of the two microtubule networks at the cortex (9).…”

Section: A Mechanical Division Rule Provides Better Predictions For Dmentioning

confidence: 99%

Cell division plane orientation based on tensile stress inArabidopsis thaliana

Louveaux

Julien

Mirabet

et al. 2016

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

165

161

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Cell geometry has long been proposed to play a key role in the orientation of symmetric cell division planes. In particular, the recently proposed Besson-Dumais rule generalizes Errera's rule and predicts that cells divide along one of the local minima of plane area. However, this rule has been tested only on tissues with rather local spherical shape and homogeneous growth. Here, we tested the application of the Besson-Dumais rule to the divisions occurring in the Arabidopsis shoot apex, which contains domains with anisotropic curvature and differential growth. We found that the Besson-Dumais rule works well in the central part of the apex, but fails to account for cell division planes in the saddle-shaped boundary region. Because curvature anisotropy and differential growth prescribe directional tensile stress in that region, we tested the putative contribution of anisotropic stress fields to cell division plane orientation at the shoot apex. To do so, we compared two division rules: geometrical (new plane along the shortest path) and mechanical (new plane along maximal tension). The mechanical division rule reproduced the enrichment of long planes observed in the boundary region. Experimental perturbation of mechanical stress pattern further supported a contribution of anisotropic tensile stress in division plane orientation. Importantly, simulations of tissues growing in an isotropic stress field, and dividing along maximal tension, provided division plane distributions comparable to those obtained with the geometrical rule. We thus propose that division plane orientation by tensile stress offers a general rule for symmetric cell division in plants.cell division plane | mechanical forces | meristem | vertex model | Arabidopsis

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“…Endoplasmic MTs are of common occurrence in premitotic cells of both lower (Brown & Lemmon, 1990ft: Panteris, Galatis & Apostolakos, 1991) and higher plants (Bakhuizen et al, 1985;Lloyd, 199! ;Wick, 1991), where they appear to connect the nucleus to the preprophase band.…”

Section: Dl'^cl Ssionmentioning

confidence: 99%

Cytoplasmic polarity and endoplasmic microtubules associated with the nucleus and organelles are ubiquitous features of food‐conducting cells in bryoid mosses (Bryophyta)

Ligrone

Duckett

1994

New Phytologist

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SUMMARYAn ultrastructural survey of food conducting cells in the gametophytes and sporophytes of bryoid mosses, including the highly specialized leptoids of Polytrichales, has revealed that, without exception, these cells have a polarized organization and contain an axial system of endoplasmic microtubules (MTs). The orientation of polarity is highly consistent with the putative direction of the source to sink gradient, with distal cellular ends, i,e, those toward the sink, containing denser cytoplasm than proximal ends. In most cases the nucleus is spindleshaped and also lies at the distal end. Longitudinal arrays of MTs are associated with the nuclear envelope. These MTs extend into the cytoplasm for long distances and may come into contact with the plasma membrane lining the terminal walls at the distal ends. Cortical MTs are absent. The endopiasmic MTs are closely associated w^ith a variety of organelles including mitochondria, plastids, endoplasmic reticulum and membrane-bounded tubules and vesicles. The organelles aligned along the MT bundles lie within longitudinal cytoplasmic strands clearly visible with light microscopy. The discovery of cytoplasmic polarity and endoplasmic MTs as distinctive features of food conducting cells of mosses sets these cells apart from the sieve elements of vascular plants. The MTorganelle associations, as observed in the food conducting cells of mosses, are hitherto undescribed in plants but are reminiscent: oi MT arrays functioning Jn organeile transport in neuronai axons and other animal and fungal systems.

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Nuclear envelope radiating microtubules in plant cells during interphase mitosis transition

Cited by 55 publications

References 20 publications

Universal rule for the symmetric division of plant cells

Universal rule for the symmetric division of plant cells

Cell division plane orientation based on tensile stress inArabidopsis thaliana

Cytoplasmic polarity and endoplasmic microtubules associated with the nucleus and organelles are ubiquitous features of food‐conducting cells in bryoid mosses (Bryophyta)

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