Division Plane Establishment and Cytokinesis

2019 ◽  
Vol 70 (1) ◽  
pp. 239-267 ◽  
Author(s):  
Pantelis Livanos ◽  
Sabine Müller
Keyword(s):  
Secretory Pathway ◽  
Preprophase Band ◽  
Cell Plate ◽  
Division Plane ◽  
Spatial Reference ◽  
Division Site ◽  
Eukaryotic Proteins ◽  
Plate Formation ◽  
Membrane Compartment ◽  
Cytoplasmic Content

Plant cells divide their cytoplasmic content by forming a new membrane compartment, the cell plate, via a rerouting of the secretory pathway toward the division plane aided by a dynamic cytoskeletal apparatus known as the phragmoplast. The phragmoplast expands centrifugally and directs the cell plate to the preselected division site at the plasma membrane to fuse with the parental wall. The division site is transiently decorated by the cytoskeletal preprophase band in preprophase and prophase, whereas a number of proteins discovered over the last decade reside continuously at the division site and provide a lasting spatial reference for phragmoplast guidance. Recent studies of membrane fusion at the cell plate have revealed the contribution of functionally conserved eukaryotic proteins to distinct stages of cell plate biogenesis and emphasize the coupling of cell plate formation with phragmoplast expansion. Together with novel findings concerning preprophase band function and the setup of the division site, cytokinesis and its spatial control remain an open-ended field with outstanding and challenging questions to resolve.

Relationship between preprophase band organization, F-actin and the division site in Allium

1990 ◽  
Vol 97 (2) ◽  
pp. 283-295
Author(s):  
Y. MINEYUKI ◽  
B. A. PALEVITZ
Keyword(s):  
Higher Plants ◽  
Preprophase Band ◽  
Cell Plate ◽  
Mitotic Apparatus ◽  
Division Plane ◽  
Division Site ◽  
Dividing Cells ◽  
G2 Phase

The preprophase band (PPB) of microtubules (Mts), which appears in the G2 phase of the cell cycle in higher plants but disappears well before the end of karyokinesis, is implicated in the determination of the division plane because its location marks the site at which the phragmoplast/cell plate will fuse with the parental plasmalemma during cytokinesis. The PPB first appears as a rather wide array, which progressively narrows before or during prophase. Actin-containing microfilaments (Mfs) have recently been reported in the PPB, but the role of these elements in PPB organization and/or function remains unclear. The present study employed fluorescence and pharmacological methods in symmetrically and asymmetrically dividing epidermal cells of Allium to probe this problem. Our results show that PPBs in cells treated with 2–200μM cytochalasin D (CD) are still transversely aligned but remain two to three times wider than mature bands in control cells. Treatment for 0.5 h at 20 μM is sufficient to make the PPBs abnormally widel Premitotic nuclear migration in asymmetrically dividing cells is also inhibited by CD, as is the positioning of the mitotic apparatus and the new cell plate. The plate is still transverse, however. Band-like arrays of cortical Mfs become evident in most interphase cells by prophase. The band remains quite wide compared to the final dimensions of the Mt PPB, and clearly encompasses it. Levels of CD as high as 200μM decrease the number of cells with transverse actin bands, although a majority still retain them. Other F-actin arrays are disrupted by the drug. Thus, while CD does not inhibit the formation of an initial, broad, transverse PPB in most cells, it does prevent the narrowing process that defines the precise division site. The role of actin in this effect is discussed.

The role of F-actin in determining the division plane of carrot suspension cells. Drug studies

Development ◽  
1988 ◽  
Vol 102 (1) ◽  
pp. 211-221 ◽  
Author(s):  
C.W. Lloyd ◽  
J.A. Traas
Keyword(s):  
Preprophase Band ◽  
Cell Plate ◽  
Suspension Cells ◽  
Mitotic Apparatus ◽  
Division Plane ◽  
Division Site ◽  
Cytoplasmic Actin ◽  
Spindle Poles ◽  
Extraction Buffer ◽  
Actin Cables

Following the report that a network of F-actin is associated with the nucleus throughout the division cycle, we have examined the involvement of F-actin in determining the division plane of carrot suspension cells. This was achieved by treating cells with drugs and then staining the unfixed cells with rhodaminyl lysine phallotoxin in detergent extraction buffer. In interphase, actin cables radiate from the nucleus but at the cortex become more or less transversely arranged in the pattern already known for cortical microtubules. Concentration of the cortical F-actin into a band at preprophase draws most of the nucleus- associated actin into a transvacuolar disc, thereby forming the phragmosome within which mitosis and cytokinesis occur. In addition to this transversely aligned structure, F-actin is also associated with the spindle poles during mitosis but these filaments tend to align at right angles to the phragmosomal actin. F-actin therefore defines transverse and longitudinal vectors as division approaches. Depolymerization of F-actin with cytochalasin D can cause the spindle axis to reorientate such that the pole-pole axis comes to lie, abnormally, parallel with the phragmosome. The cytokinetic apparatus (the phragmoplast) develops centrifugally within the phragmosome. There has been considerable speculation on the nature of the elements that guide the phragmoplast to the cortical site previously occupied by the preprophase band of microtubules. This study demonstrates that F-actin bridges the leading margin of the outgrowing phragmoplast to the opposing cortex. Radial actin strands therefore provide a ‘memory’ of the predetermined division plane whose perimeter had been marked at preprophase by a band composed of microtubules and F-actin. This relationship was perturbed with the herbicide, chloroisopropylphenyl carbamate. Preprophase bands of actin appear to form normally in herbicide-treated cells. However, cytokinesis does not occur within this predicted plane since the drug perturbs the mitotic spindle, forming three nuclei which become separated by Y-shaped, actin-containing phragmoplasts. Cytoplasmic actin strands connect the edges of the phragmoplast to the cortex. It is suggested that the irregular distribution of F-actin, which radiates from the herbicide-altered mitotic apparatus, provides alternative paths for outgrowth of the abnormal phragmoplasts. Caffeine is known to cause failure of cell plate formation. But apart from inducing cytoplasmic ‘starbursts’ of F-actin in interphase cells it does not appear to have any effect on F-actin-containing division structures. It is concluded that the formation of a transvacuolar phragmosome, spindle alignment and the ‘correct’ outgrowth of a planar cytokinetic apparatus to the predetermined boundary of the division site all involve F-actin.

scholarly journals Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis

2001 ◽  
Vol 155 (2) ◽  
pp. 239-250 ◽  
Author(s):  
Maren Heese ◽  
Xavier Gansel ◽  
Liliane Sticher ◽  
Peter Wick ◽  
Markus Grebe ◽  
...  
Keyword(s):  
Cell Division ◽  
Membrane Fusion ◽  
Functional Characterization ◽  
Cell Plate ◽  
Yeast Two Hybrid ◽  
Division Plane ◽  
Plant Cytokinesis ◽  
Cell Plate Formation ◽  
Plate Formation ◽  
Two Hybrid

Cytokinesis requires membrane fusion during cleavage-furrow ingression in animals and cell plate formation in plants. In Arabidopsis, the Sec1 homologue KEULE (KEU) and the cytokinesis-specific syntaxin KNOLLE (KN) cooperate to promote vesicle fusion in the cell division plane. Here, we characterize AtSNAP33, an Arabidopsis homologue of the t-SNARE SNAP25, that was identified as a KN interactor in a yeast two-hybrid screen. AtSNAP33 is a ubiquitously expressed membrane-associated protein that accumulated at the plasma membrane and during cell division colocalized with KN at the forming cell plate. A T-DNA insertion in the AtSNAP33 gene caused loss of AtSNAP33 function, resulting in a lethal dwarf phenotype. atsnap33 plantlets gradually developed large necrotic lesions on cotyledons and rosette leaves, resembling pathogen-induced cellular responses, and eventually died before flowering. In addition, mutant seedlings displayed cytokinetic defects, and atsnap33 in combination with the cytokinesis mutant keu was embryo lethal. Analysis of the Arabidopsis genome revealed two further SNAP25-like proteins that also interacted with KN in the yeast two-hybrid assay. Our results suggest that AtSNAP33, the first SNAP25 homologue characterized in plants, is involved in diverse membrane fusion processes, including cell plate formation, and that AtSNAP33 function in cytokinesis may be replaced partially by other SNAP25 homologues.

scholarly journals Pollen Development in Orchids. 5. A Generative Cell Domain Involved in Spatial Control of the Hemispherical Cell Plate

1991 ◽  
Vol 100 (3) ◽  
pp. 559-565
Author(s):  
R. C. BROWN ◽  
B. E. LEMMON
Keyword(s):  
Generative Cell ◽  
Preprophase Band ◽  
Cell Plate ◽  
Generative Nucleus ◽  
Pollen Mitosis ◽  
Spatial Control ◽  
Division Plane ◽  
Radial System ◽  
Vegetative Pole ◽  
First Pollen Mitosis

The unequal first pollen mitosis in moth orchids (Phalaenopsis) is followed by an unusual form of cytokinesis that isolates a small lens-shaped generative cell from a large vegetative cell. No preprophase band of microtubules predicts the division plane and the new cell plate grows completely around the generative cell rather than fusing with the parental wall. Development of the phragmoplast cytoskeleton consisting of fusiform bundles of microtubules and F-actin occurs in three major stages: (1) the initial asymmetrical phragmoplast conforming to the shape of the interzonal region, which tapers from the broad mass of chromosomes at the generative pole to the rounded mass at the vegetative pole; (2) the symmetrical plate-like phragmoplast; and (3) the hemispherical phragmoplast, which curves around the generative nucleus. Microtubules of the generative half of the hemispherical phragmoplast are nuclearbased, while those on the vegetative side terminate in endoplasmic reticulum. The path of the phragmoplast appears to outline a cytoplasmic domain denned by a radial system of microtubules emanating from the generative nucleus.

scholarly journals SABRE populates ER domains essential for cell plate maturation and cell expansion influencing cell and tissue patterning

2020 ◽  
Author(s):  
Xiaohang Cheng ◽  
Magdalena Bezanilla
Keyword(s):  
Cell Expansion ◽  
Cell Biology ◽  
Cell Plate ◽  
Genetic Alterations ◽  
Callose Deposition ◽  
Division Plane ◽  
Cell Plate Formation ◽  
Tissue Patterning ◽  
Plate Formation ◽  
In Cells

AbstractThe SABRE protein, originally identified in plants, is found throughout eukaryotes. In plants, SABRE has been implicated in cell expansion, division plane orientation and planar polarity. However, how SABRE mediates these processes remains an open question. Here, we have taken advantage of the fact that the bryophyte Physcomitrium patens has a single copy of SABRE, is an excellent model for cell biology and is readily amenable to precise genetic alterations to investigate SABRE’s mechanism of action. We discovered that SABRE null mutants were stunted in both polarized growing and diffusely growing tissues, similar to reported phenotypes in seed plants. However, in polarized growing cells, we observed significant delays in cell plate formation and sometimes catastrophic failures in cell division. We generated a functional SABRE fluorescent fusion protein and determined that it forms dynamic puncta on regions of the endoplasmic reticulum (ER) both in the cytoplasm during interphase and at the new cell plate during division. In the absence of SABRE, ER morphology was severely compromised with large aggregates accumulating in the cytoplasm and abnormal buckling along the developing cell plate late in cytokinesis. In fact, SABRE and the ER maximally accumulated on the developing plate specifically during cell plate maturation, coincident with the timing of the onset of failures in cell plate formation in cells lacking SABRE. Further we discovered that callose deposition is delayed in Δsabre cells, and in cells that failed to divide, abnormal callose accumulations formed at the cell plate. Our findings demonstrated that SABRE functions by influencing the ER and callose deposition, revealing a surprising and essential role for the ER in cell plate maturation. Given that SABRE is conserved, understanding how SABRE influences cell and tissue patterning has profound significance across eukaryotes.

scholarly journals TANGLED1 mediates interactions between microtubules that may promote spindle organization and phragmoplast guidance to the division site in maize

2019 ◽  
Author(s):  
Pablo Martinez ◽  
Ram Dixit ◽  
Rachappa S. Balkunde ◽  
Seán E. O’Leary ◽  
Kenneth A. Brakke ◽  
...  
Keyword(s):  
Critical Role ◽  
Preprophase Band ◽  
Microtubule Organization ◽  
Division Plane ◽  
Plane Orientation ◽  
Division Site ◽  
Structural Framework ◽  
Cell Shapes ◽  
Division Plane Orientation

AbstractThe microtubule cytoskeleton serves as a dynamic structural framework for mitosis in eukaryotic cells. TANGLED1 (TAN1) is a microtubule-binding protein that localizes to the division site and mitotic microtubules and plays a critical role in division plane orientation in plants. Here, in vitro experiments demonstrate that TAN1 directly binds microtubules, mediating microtubule zippering or end-on microtubule interactions, depending on their contact angle. Maize tan1 mutant cells improperly position the preprophase band (PPB), which predicts the future division site. However, cell-shape-based modeling indicates that PPB positioning defects are likely a consequence of abnormal cell shapes and not due to TAN1 absence. Spindle defects in the tan1 mutant suggest that TAN1-mediated microtubule zippering may contribute to metaphase spindle organization. In telophase, co-localization of growing microtubules ends from the phragmoplast with TAN1 at the division site suggests that TAN1 interacts with microtubule tips end-on. Together, our results suggest that TAN1 contributes to spindle and phragmoplast microtubule organization to ensure proper division plane orientation.

scholarly journals TANGLED1 mediates microtubule interactions that may promote division plane positioning in maize

2020 ◽  
Vol 219 (8) ◽  
Author(s):  
Pablo Martinez ◽  
Ram Dixit ◽  
Rachappa S. Balkunde ◽  
Antonia Zhang ◽  
Seán E. O’Leary ◽  
...  
Keyword(s):  
Critical Role ◽  
Preprophase Band ◽  
Microtubule Organization ◽  
Division Plane ◽  
Plane Orientation ◽  
Division Site ◽  
Structural Framework ◽  
Cell Shapes ◽  
Division Plane Orientation

The microtubule cytoskeleton serves as a dynamic structural framework for mitosis in eukaryotic cells. TANGLED1 (TAN1) is a microtubule-binding protein that localizes to the division site and mitotic microtubules and plays a critical role in division plane orientation in plants. Here, in vitro experiments demonstrate that TAN1 directly binds microtubules, mediating microtubule zippering or end-on microtubule interactions, depending on their contact angle. Maize tan1 mutant cells improperly position the preprophase band (PPB), which predicts the future division site. However, cell shape–based modeling indicates that PPB positioning defects are likely a consequence of abnormal cell shapes and not due to TAN1 absence. In telophase, colocalization of growing microtubules ends from the phragmoplast with TAN1 at the division site suggests that TAN1 interacts with microtubule tips end-on. Together, our results suggest that TAN1 contributes to microtubule organization to ensure proper division plane orientation.

Microtubule and F-actin dynamics at the division site in living Tradescantia stamen hair cells

1992 ◽  
Vol 103 (4) ◽  
pp. 977-988 ◽  
Author(s):  
A.L. Cleary ◽  
B.E.S. Gunning ◽  
G.O. Wasteneys ◽  
P.K. Hepler
Keyword(s):  
Hair Cells ◽  
Preprophase Band ◽  
Cell Plate ◽  
Laser Scanning Microscopy ◽  
Actin Dynamics ◽  
Cell Cortex ◽  
Living Plant ◽  
Rhodamine Phalloidin ◽  
Division Site ◽  
The Future

We have visualised F-actin and microtubules in living Tradescantia virginiana stamen hair cells by confocal laser scanning microscopy after microinjecting rhodamine-phalloidin or carboxyfluorescein-labelled brain tubulin. We monitored these components of the cytoskeleton as the cells prepared for division at preprophase and progressed through mitosis to cytokinesis. Reorganisation of the interphase cortical cytoskeleton results in preprophase bands of both F-actin and microtubules that coexist in the cell cortex, centred on the site at which the future cell plate will fuse with the parent cell wall. The preprophase band of microtubules is formed from microtubules that polymerise and incorporate tubulin during prophase. The preprophase band of actin may form either by reorganisation of pre-existing filaments or by de novo polymerisation. Both cytoskeletal components disappear from the future division site approximately five minutes prior to the breakdown of the nuclear envelope. Cortical microtubules are undetectable throughout mitosis and cytokinesis, whereas cortical F-actin remains abundant, although it is notably excluded from the division site. The phragmoplast, containing both F-actin and microtubules, expands towards the cortical actin exclusion-zone through a region that has no detectable microtubules or F-actin. The phragmoplast comes to rest in the predefined region of the cortex that is devoid of F-actin. It is proposed that cortical F-actin may act as a “negative” template which could position the phragmoplast and cell plate correctly. This is the first in vivo documentation of F- actin dynamics at the division site in living plant cells.

Plant cytokinesis: a tale of membrane traffic and fusion

2015 ◽  
Vol 43 (1) ◽  
pp. 73-78 ◽  
Author(s):  
Gerd Jürgens ◽  
Misoon Park ◽  
Sandra Richter ◽  
Sonja Touihri ◽  
Cornelia Krause ◽  
...  
Keyword(s):  
Higher Plants ◽  
Membrane Vesicles ◽  
Cell Plate ◽  
Division Plane ◽  
Daughter Cells ◽  
Division Site ◽  
Plant Cytokinesis ◽  
M Phase ◽  
Golgi Network ◽  
Sm Protein

Cytokinesis separates the forming daughter cells. Higher plants have lost the ability to constrict the plasma membrane (PM) in the division plane. Instead, trans-Golgi network (TGN)-derived membrane vesicles are targeted to the centre of the division plane and generate, by homotypic fusion, the partitioning membrane named cell plate (CP). The CP expands in a centrifugal fashion until its margin fuses with the PM at the cortical division site. Mutant screens in Arabidopsis have identified a cytokinesis-specific syntaxin named KNOLLE and an interacting Sec1/Munc18 (SM) protein named KEULE both of which are required for vesicle fusion during cytokinesis. KNOLLE is only made during M-phase, targeted to the division plane and degraded in the vacuole at the end of cytokinesis. Here we address mechanisms of KNOLLE trafficking and interaction of KNOLLE with different soluble N-ethylmaleimide-sensitive factor (NSF) attachment protein (SNAP) receptor (SNARE) partners and with SM-protein KEULE, ensuring membrane fusion in cytokinesis.

scholarly journals Predicting division planes of three-dimensional cells by soap-film minimization

2017 ◽  
Author(s):  
Pablo Martinez ◽  
Lindy A. Allsman ◽  
Kenneth A. Brakke ◽  
Christopher Hoyt ◽  
Jordan Hayes ◽  
...  
Keyword(s):  
Developmental Regulation ◽  
Three Dimensional ◽  
Soap Film ◽  
Preprophase Band ◽  
Animal Cells ◽  
Division Plane ◽  
Plane Orientation ◽  
Division Site ◽  
Division Plane Orientation

AbstractOne key aspect of cell division in multicellular organisms is the orientation of the division plane. Proper division plane establishment contributes to normal organization of the plant body. To determine the importance of cell geometry in division plane orientation, we designed a threedimensional probabilistic mathematical modeling approach to directly test the century-old hypothesis that cell divisions mimic “soap-film minima” or that daughter cells have equal volume and the resulting division plane is a local surface area minimum. Predicted division planes were compared to a plant microtubule array that marks the division site, the preprophase band (PPB). PPB location typically matched one of the predicted divisions. Predicted divisions offset from the PPB occurred when a neighboring cell wall or PPB was observed directly adjacent to the predicted division site, to avoid creating a potentially structurally unfavorable four-way junction. By comparing divisions of differently shaped plant and animal cells to divisions simulated in silico, we demonstrate the generality of this model to accurately predict in vivo division. This powerful model can be used to separate the contribution of geometry from mechanical stresses or developmental regulation in predicting division plane orientation.

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