Laser microsurgery demonstrates that cytoplasmic strands anchoring the nucleus across the vacuole of premitotic plant cells are under tension. Implications for division plane alignment (original) (raw)

Nucleus-associated microtubules help determine the division plane of plant epidermal cells: avoidance of four-way junctions and the role of cell geometry

The Journal of cell …, 1990

To investigate the spatial relationship between the nucleus and the cortical division site, epidermal cells were selected in which the separation between these two areas is large. Avoiding enzyme treatment and air drying, Datura stramonium cells were labeled with antitubulin antibodies and the threedimensional aspect of the cytoskeletons was reconstructed using computer-aided optical sectioning. In vacuolated cells preparing for division, the nucleus migrates into the center of the cell, suspended by transvacuolar strands. These strands are now shown to contain continuous bundles of microtubules which bridge the nucleus to the cortex. These nucleus-radiating microtubules adopt different configurations in cells of different shape. In elongated cells with more or less parallel side walls, oblique strands radiating from the nucleus to the long side walls are presumably unstable, for they are progressively realigned into a transverse disc (the phragmosome) as broad, cortical, preprophase bands (PPBs) become tighter. The phragmosome and the PPB are both known predictors of the division plane and our observations indicate that they align simultaneously in elongated epidermal cells. These observations suggest another hypothesis: that the PPB may contain microtubules polymerized from the nuclear surface. In elongated cells, the majority of the radiating microtubules, therefore, come to anchor the nucleus in the transverse plane, consistent

Plant Cytoskeleton: Reinforcing Lines of Division in Plant Cells

Current Biology, 2004

Cytokinesis in plants has unique features concerned with defining and maintaining the line of cell division. Recent studies have identified key cytoskeletal components and events that help to ensure the fidelity of cytokinesis in higher plants. The ability to divide is a fundamental property of living cells. In plants, the presence of a cell wall and absence of cell migration makes the establishment of the line of division between daughter cells a critical step, important for both organ morphogenesis and the overall architecture of the plant body. Somatic cell cytokinesis in higher plants thus presents certain unique features [1]. Following a stage known as karyokinesis, in which the cell undergoes nuclear division, a distinct cytoplasmic domain-the phragmoplast-is defined between the reforming nuclei. The ring-like phragmoplast effectively demarcates the 'division plane' as it mediates organelle and vesicular traffic to orchestrate the assembly of a growing cell-plate that fragments the cell into two. Intriguingly, in most dividing plant cells the site of phragmoplast formation, and thereby the future division plane, is predicted accurately, well in advance of other cell-division events, by a transiently occurring 'pre-prophase band' [1,2]. The pre-prophase band disappears completely by pro-metaphase, and is thus temporally well separated from the phragmoplast assembly that typically occurs during late anaphase. However, the coincident localization of the preprophase band and the phragmoplast suggest that the former leaves some sort of imprint in the parent cell's memory. The search for this imprint led to the identification of another intracellular zone defined between the stages of pre-prophase band and phragmoplast formation. This 'actin-depleted zone' apparently provides a spatial reference site for the phragmoplast and may constitute the 'memory' left behind by the pre-prophase band [3]. The pre-prophase band, actin-depletion zone and the phragmoplast (Figure 1) thus constitute major arrays that define the division line, and their creation and maintenance obviously plays an important role in cytokinesis. But despite excellent descriptions emphasizing their spatio-temporal relationship and interdependence, not much is known about the molecular factors involved in their creation and maintenance. Recent studies [4-11] have identified many of the molecular components that play pivotal roles in generating and/or reinforcing these cytoplasmic landmarks, and provided fresh insights into the novel cytokinesis process in plants.

Symmetric reorganizations of radiating microtubules around pre- and post-mitotic nuclei of dividing cells organized within intact root meristems

Journal of Plant Physiology, 1996

Using indirect immunofluorescence, the system of radiating endoplasmic microtubules (REMTs) within intact cells of meristematic root tissues of maize has been examined throughout the cell cycle, paying special attention to its relationship with the pre-and post-mitotic nuclei with which it is associated. At early interphase, REMTs are not uniformly disposed around the nucleus but grow out from faint, though easily recognizable, perinuclear foci. During S and G2 phases, REMTs increase in number and have a close association with the assembly of the preprophase band (PPB) MT array. Later, when the cortical part of the PPB disintegrates, the REMTs align along the nuclear surface, predicting the long axis of the future mitotic spindle. In contrast to naturally wall-less cells, or to cells with perturbed cell walls, these pre-mitotic, as well as the subsequently formed post-mitotic cells display symmetrical rearrangements of their REMTs around the nuclear surface. Mitotic cells sectioned in the median plane show a symmetrical quadripolar MT organization which is obvious at all stages of mitosis. The symmetrical redistributions of the REMTs which occur during the cell cycle are perturbed, or even prevented, by treatments with chemical or with physical anti-MT agents. Nuclei of cells so treated accumulate REMTs, but fail to redistribute them symmetrically. As a result, the pre-and post-mitotic nuclei of root cells treated with anti-MT agents resemble, with respect to their REMTs, the corresponding nuclei of wall-less plant cells, or of cells which have perturbed cell walls. The dynamic REMTs which connect the pre-and post-mitotic nuclei with the cell periphery are suggested as being involved in sensing the position of dividing cells within the intact plant organ. This property of REMTs enables them to spatially control the sequential alignment of cell division planes of immobile walled plant cells which underlies the morphogenesis of higher plant organs.

Plant nuclei can contain extensive grooves and invaginations

The Plant Cell

Plant cells can exhibit highly complex nuclear organization. Through dye-labeling experiments in untransformed onion epidermal and tobacco culture cells and through the expression of green fluorescent protein targeted to either the nucleus or the lumen of the endoplasmic reticulum/nuclear envelope in these cells, we have visualized deep grooves and invaginations into the large nuclei of these cells. In onion, these structures, which are similar to invaginations seen in some animal cells, form tubular or planelike infoldings of the nuclear envelope. Both grooves and invaginations are stable structures, and both have cytoplasmic cores containing actin bundles that can support cytoplasmic streaming. In dividing tobacco cells, invaginations seem to form during cell division, possibly from strands of the endoplasmic reticulum trapped in the reforming nucleus. The substantial increase in nuclear surface area resulting from these grooves and invaginations, their apparent preference for ass...

The plant cell body: a cytoskeletal tool for cellular development and morphogenesis

Protoplasma, 1998

Certain aspects of cellular behaviour in relation to growth and development of plants can be understood in terms of the "cell body" concept proposed by Daniel Mazia in 1993. During the interphase of the mitotic cell cycle, the plant cell body is held to consist of a nucleus and a perinuclear microtubule-organizing centre from which microtubules radiate into the cytoplasm. During mitosis and cytokinesis in meristematic cells, and also during the period of growth in post-mitotic cells immediately beyond the meristem, the plant cell body undergoes various characteristic morphological transformations, "many of which are proposed as being related to changing structural connections with the actin-based component of the cytoskeleton and with specialized, plasma-membrane-associated sites at the cell periphery. In post-mitotic cells, these transformations of the plant cell body coincide with, and probably provide conditions for, the various pathways of development which such cells follow. They are also responsible for the acquisition of new cellular polarities. Events in which the plant cell body participates include the formation of a mitotic spindle, phragmoplast, and new cell division wall, the rearrangement of a diffuse type of cell wall growth into tip growth (as occurs, e.g., during the initiation and subsequent development of root hairs), and the growth and division that occurs in reactivated vacuolate cells. If more evidence can be marshalled in support of the existence and properties of the plant cell body, then this concept could prove useful in interpreting the cytological bases of a range of developmental events in plants.

Demarcation of the cortical division zone in dividing plant cells

Cell Biology International, 2008

Somatic cytokinesis in higher plants involves, besides the actual construction of a new cell wall, also the determination of a division zone. Several proteins have been shown to play a part in the mechanism that somatic plant cells use to control the positioning of the new cell wall. Plant cells determine the division zone at an early stage of cell division and use a transient microtubular structure, the preprophase band (PPB), during this process. The PPB is formed at the division zone, leaving behind a mark that during cytokinesis is utilized by the phragmoplast to guide the expanding cell plate toward the correct cortical insertion site. This review discusses old and new observations with regard to mechanisms implicated in the orientation of cell division and determination of a cortical division zone. Ó

Microfilaments: dynamic arrays in higher plant cells

Journal of Cell Biology, 1987

By using fluorescently labeled phalloidin we have examined, at the light microscope level, the three-dimensional distribution and reorganization of actin-like microfilaments (mfs) during plant cell cycle and differentiation. At interphase, mfs are organized into three distinct yet interconnected arrays: (a) fine peripheral networks close to the plasma membrane; (b) large axially oriented cables in the subcortical region; (c) a nuclear "basket" of mfs extending into the transvacuolar strands. All these arrays, beginning with the peripheral network, disappear at the onset of mitosis and reappear, beginning with the nuclear basket, after cytokinesis. During mitotic and cytokinetic events, mfs are associated with the spindle and phragmoplast. Actin staining in the spindle is localized between the chromosomes and the spindle poles and changes in a functionally specific manner. The nuclear region appears to be the center for mf organization and/or initiation. During differentiation from rapid cell division to cell elongation, mf arrays switch from an axial to a transverse orientation, thus paralleling the microtubules. This change in orientation reflects a shift in the direction of cytoplasmic streaming. These observations show for the first time that actin-like mfs form intricate and dynamic arrays in plant cells which may be involved in many as yet undescribed cell functions.

Polarized endoplasmic reticulum aggregations in the establishing division plane of protodermal cells of the fern Asplenium nidus

Protoplasma, 2014

The determination of the division plane in protodermal cells of the fern Asplenium nidus occurs during interphase with the formation of the phragmosome, the organization of which is controlled by the actomyosin system. Usually, the phragmosomes between adjacent cells were oriented on the same plane. In the phragmosomal cortical cytoplasm, an interphase microtubule (MT) ring was formed and large quantities of endoplasmic reticulum (ER) membranes were gathered, forming an interphase U-like ER bundle. During preprophase/prophase, the interphase MT ring and the U-like ER bundle were transformed into a MT and an ER preprophase band (PPB), respectively. Parts of the ER-PPB were maintained during mitosis. Furthermore, the plasmalemma as well as the nuclear envelope displayed local polarization on the phragmosome plane, while the cytoplasm between them was occupied by distinct ER aggregations. These consistent findings suggest that Α. nidus protodermal cells constitute a unique system in which three elements of the endomembrane system (ER, plasmalemma, and nuclear envelope) show specific characteristics in the establishing division plane. Our experimental data support that the organization of the U-like ER bundle is controlled on a cellular level by the actomyosin system and intercellularly by factors emitted from the leaf apex. The possible role of the above endomembrane system elements on the mechanism that coordinates the determination of the division plane between adjacent cells in protodermal tissue of A. nidus is discussed.