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WIREs Dev Biol
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Mechanisms of plant cell division

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Plant cells are confined by a network of cellulosic walls that imposes rigid control over the selection of division plane orientations, crucial for morphogenesis and genetically regulated. While in animal cells and yeast, the actin cytoskeleton is instrumental in the execution of cytokinesis, in plant cells the microtubule cytoskeleton is taking the lead in spatially controlling and executing cytokinesis by the formation of two unique, plant‐specific arrays, the preprophase band (PPB) and the phragmoplast. The formation of microtubule arrays in plant cells is contingent on acentrosomal microtubule nucleation. At the onset of mitosis, the PPB defines the plane of cell division where the partitioning cell wall is later constructed by the cytokinetic phragmoplast, imposing a spatio‐temporal relationship between the two processes. Current research progress in the field of plant cell division focuses on identifying and tying the links between early and late events in spatial control of cytokinesis and how microtubule array formation is regulated in plant cells. WIREs Dev Biol 2015, 4:391–405. doi: 10.1002/wdev.186 This article is categorized under: Plant Development > Vegetative Development
Micrographs of the microtubule arrays during plant cell division. Mitotic cell cycle stages are depicted in chronological order. Microtubules are visualized by GFP‐MBD, depicted in green, cell walls are stained with propidium iodide (magenta). Maximum projections of GFP‐MBD z‐stacks are merged with a single propidium iodide image. In case where images were rotated, non‐imaged regions were filled with black background. Scale bar indicates 10 µm.
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Regulation and mechanisms of phragmoplast expansion. HIK/NACK kinesin (blue) binding to a MAPKKK increases the kinase activity, to activate the NACK‐PQR MAPK (green gradient) signaling cascade that targets MAP65 proteins. In metaphase, the NACK/HINKEL‐dependent mitogen‐activated protein kinase (MAPK) signaling cascade is inhibited by CDK‐dependent phosphorylation of the kinesin NACK1 and the MAPK kinase kinase NPK1 (dark green). During cell cycle progression CDK activity is switched off, allowing the accumulation of non‐phosphorylated NPK1 that eventually binds to non‐phosphorylated NACK1 in the phragmoplast midzone regions. This complex formation triggers the kinase cascade, which targets MAP65 proteins at the trailing edge of the phragmoplast. Phosphorylation of MAP65 inhibits its cross‐linking activity toward antiparallel microtubules. Consequently microtubules at the trailing edge become destabilized and disassemble, discharging tubulin heterodimers. At the leading edge of the phragmoplast, new, dynamic microtubules nucleate on existing microtubules at an angle around 40°. γ‐Tubulin containing nucleation sites move toward microtubule minus ends as they polymerize new microtubules. Antiparallel dynamic microtubules are bundled by MAP65. Progressively, the leading edge expands laterally allowing new vesicle fusion. At the trailing edge, where cell plate formation is completed, microtubules depolymerize.
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Illustration of the actin cytoskeleton and selected associated proteins in plant mitosis. F‐actin (blue) is a component of the preprophase band (PPB) but not restricted to it. Actin bundles span throughout the entire cell. Upon PPB disassembly in prometaphase, the region of the cortical division zone (CDZ) remains almost devoid of F‐actin, but is flanked by actin enrichments, also referred to as twin peaks. The kinesin‐14 KCA1 (purple dashed line) decorates the cell cortex but is depleted from the CDZ. Myo8 (red) associates with microtubules and localizes to the spindle poles and spindle midzone. During anaphase, Myo8 locates exclusively to microtubule overlaps in the spindle midzone and also accumulates at the CDZ. During cytokinesis, Myo8 remains associated with dynamic phragmoplast microtubules at the leading edge and with peripheral microtubules that seem to contact the CDS. These peripheral microtubules move toward the leading phragmoplast edge. It is hypothesized that Myo8 might use actin filaments spanning the distance between the phragmoplast and the CDS for the relocation of the peripheral microtubules. F‐actin is indeed present between the phragmoplast and the CDS and furthermore, actin nucleating formin For2a (orange) accumulates in the phragmoplast midzone, further supporting the notion that Myo8 acts in a mechanism to maintain phragmoplast integrity.
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Schematic illustration of plant spindle formation. (a) Cell cycle stages are illustrated as cell cross sections, while interphase is depicted as a projection. Perinuclear microtubules emanate from the nucleus and bridging microtubules (green) connect the nucleus and the preprophase band (PPB green dashed line) in late prophase. The MAP TPX2, which accumulates in the nucleus during preprophase (blue gradient), is exported and associates with AURORA (AUR) 1 at the nuclear envelope (AUR1/TPX2 complex purple). During nuclear envelope breakdown (purple dashed line), the AUR1/TPX2 complex localizes to minus ends of perinuclear microtubules and subsequently colocalizes with spindle poles and accumulates at the spindle, presumably co‐localizing with microtubule nucleation complexes. Note that the AUR1/TPX2 complex especially localizes at kinetochore microtubules during the transition from metaphase to anaphase. Whereas TPX2 rapidly disappears at the end of anaphase, AUR1 decorates the cell plate during cytokinesis (pink). Kinesin‐14 ATK5 (yellow) colocalizes with perinuclear microtubules in preprophase/prophase and associates with antiparallel interpolar microtubules at the spindle midzone. During cytokinesis, ATK5 assembles at the phragmoplast midzone. (b) Microtubule plus end association of ATK5 is mediated through its C‐terminal tail domain, while microtubule minus‐end‐directed mobility requires ATK5 motor domain.
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Protein dynamics at the cortical division site (CDS). (a) Selection of proteins that are required for preprophase band (PPB) formation, positioning, and cortical division zone (CDZ) establishment is depicted. Proteins of the TTP (TON1/TRM/PP2A, red) complex localize at the PPB and are required for its formation. CLASP (dark green) and SABRE (SAB, purple) genetically interact to position the PPB, although CLASP colocalizes with the PPB, SAB is located at its lateral boundaries. In prophase, the proteins POK1 (mint), TANGLED (TAN, blue), and RanGAP1 (yellow) are independently recruited to the PPB and remain at this cortical site beyond PPB disassembly. In metaphase POK1 is somehow tethered to the CDZ and retains TAN and RanGAP1 at this site throughout mitosis. In cytokinesis, the localization of POK1, TAN, and RanGAP1 becomes narrow, most likely more accurately describing the site of cell plate fusion or CDS. Note that RanGAP1 also associates with the nuclear envelope in prophase and with kinetochores and the cell plate later in mitosis. (b) Interaction network of the above featured proteins at the PPB/CDZ as determined either by biochemical evidence (continuous line) or by genetic evidence. The TPP complex consists of protein phosphatase 2A variable scaffolding A subunit, the regulatory B subunit (FASS), and the variable catalytic C subunit as well as the assembly activator TONNEAU (TON) 1a/b and variable TONNEAU1 RECRUITING MOTIF (TRM) proteins. TRM interacts with FASS via the conserved M2 motif, and the interaction of TON1 with TRM M3 motif mediates cytoskeletal targeting. Localization of TAN and RanGAP1 at the PPB depends on FASS.
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Overview of cortical division site (CDS) establishment and maintenance. Entry into mitosis is under the control of the cell cycle. The transition from G2 phase to mitosis (M) is mediated by the CDKA;CYCB complex. The nucleus (green) gets centered as the cell enters mitosis and the preprophase band (PPB, blue) subsequently assembles depending on TTP (TON1/TRM/PP2A) protein complex and phosphatase activity. A number of MAPs colocalize with the PPB and direct its position (SABRE, CLASP, MOR1, KTN1, MAPs). The PPB accurately predicts the future cell plate insertion site. Mutation of proteins involved in PPB assembly leads to loss of PPB formation and in consequence mispositioned cell walls. In the presence of PPB, TANGLED (TAN), RANGAP1, and POK1 are recruited to the PPB during prophase, establishing the cortical division zone (CDZ). The purple color indicates the co‐localization of PPB microtubules and positive CDZ markers during prometaphase. Upon PPB disassembly, the CDZ (red) preserves the positional information conveyed by the PPB. POK1 is required for the maintenance of TAN and RanGAP1 commencing in metaphase. The loss of POKs, TAN, F‐actin, and Myo8 leads to obliquely inserted cell walls, whereas knock down of RanGAP function causes incomplete cell walls. During cytokinesis, the CDZ (including its residents) narrows to define CDS as the precise cell plate insertion site. POK1 and Myo8 are required for phragmoplast guidance toward the CDS. Upon completion of cell plate insertion, CDS markers disappear.
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Regulation of division plane positioning in symmetric and asymmetric divisions. (a) Succession of divisions in the early Arabidopsis embryo. Chronologically invariant symmetric and asymmetric divisions contribute to normal development of globular stage embryos. Symmetric divisions give rise to the eight‐cell embryo (indicated in red) obeying the geometric rule of minimal area division, while highly asymmetric divisions facilitate the separation of outer protoderm and inner cell types at the transition from 8‐ to 16‐cell stage (indicated in green). Auxin signaling overrides default symmetric divisions, allowing asymmetric divisions. Changes in auxin response result in reversion to the geometry‐based symmetric default pathway. 3D reconstruction illustrates the default minimum area division plane (red) in comparison to an asymmetric division plane (green) at the transition from 8‐ to 16‐cell stage. (b) Model for the transcription factor regulated control of asymmetric division in the stomatal lineage. SPEECHLESS (SPCH, green) regulates both transcription of BASL and kinesin ARK3/KINUa in a meristemoide cell. SPCH preceeds ARK3 (purple) localization at the preprophase band (PPB), while BASL localizes at the plasma membrane opposing the imminent future division site, acting as a polarity cue. Presumably, BASL and ARK3/KINUa act in the same genetic pathway, yet the interdependency of their subcellular location needs to be clarified.
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