The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell division

Abstract

The unique cytokinetic apparatus of higher plant cells comprises two cytoskeletal systems: a predictive preprophase band of microtubules (MTs), which defines the future division site, and the phragmoplast, which mediates crosswall formation after mitosis. We review features of plant cell division in an evolutionary context and from the viewpoint that the cell is a domain of cytoplasm (cytoplast) organized around the nucleus by a cytoskeleton consisting of a single "tensegral" unit. The term "tensegrity" is a contraction of "tensional integrity" and the concept proposes that the whole cell is organized by an integrated cytoskeleton of tension elements (e.g., actin fibers) extended over compression-resistant elements (e.g., MTs).During cell division, a primary role of the spindle is seen as generating two cytoplasts from one with separation of chromosomes a later, derived function. The telophase spindle separates the newly forming cytoplasts and the overlap between half spindles (the shared edge of two new domains) dictates the position at which cytokinesis occurs. Wall MTs of higher plant cells, like the MT cytoskeleton in animal and protistan cells, spatially define the interphase cytoplast. Redeployment of actin and MTs into the preprophase band (PPB) is the overt signal that the boundary between two nascent cytoplasts has been delineated. The "actin-depleted zone" that marks the site of the PPB throughout mitosis may be a more persistent manifestation of this delineation of two domains of cortical actin. The growth of the phragmoplast is controlled by these domains, not just by the spindle. These domains play a major role in controlling the path of phragmoplast expansion. Primitive land plants show different morphological changes that reveal that the plane of division, with or without the PPB, has been determined well in advance of mitosis.The green alga Spirogyra suggests how the phragmoplast system might have evolved: cytokinesis starts with cleavage and then actin-related determinants stimulate and positionally control cell-plate formation in a phragmoplast arising from interzonal MTs from the spindle. Actin in the PPB of higher plants may be assembling into a potential furrow, imprinting a cleavage site whose persistent determinants (perhaps actin) align the outgrowing edge of the phragmoplast, as in Spirogyra. Cytochalasin spatially disrupts polarized mitosis and positioning of the phragmoplast. Thus, the tensegral interaction of actin with MTs (at the spindle pole and in the phragmoplast) is critical to morphogenesis, just as they seem to be during division of animal cells. In advanced green plants, intercalary expansion driven by turgor is controlled by MTs, which in conjunction with actin, may act as stress detectors, thereby affecting the plane of division (a response clearly evident after wounding of tissue). The PPB might be one manifestation of this strain detection apparatus.

Allelopathy of Aquatic Autotrophs

“…Most hydrolyzable polyphenols effectively complex proteins, and thus might inhibit enzymes (Haslam, 1989). The occurrence of hydrolyzable polyphenols in chlorophytes is limited to species belonging to the 'phragmoplast' group (see Sawitzky and Grolig, 1995;Pickett-Heaps et al, 1999) such as Spirogyra. Tannins are stored in vacuoles of this filamentous chlorophyte, comparable to higher plants.…”

Microtubule networks for plant cell division

“…During cellularization of certain multinucleated plant cells, spindles do not precede phragmoplast assembly. However, here another bipolar microtubule array is reported to form between nuclear surfaces to act as a precursor for the phragmoplast (Van Lammeren et al 1985;reviewed in Otegui and Staehelin 2000;Pickett-heaps et al 1999;De Storme and Geelen 2013). Thus, in general, the phragmoplast maintains the bipolarity that is established by a preceding microtubule structure.…”

Phylogenesis, Origin and Kinship of the Charophytic Algae

“…However,insomemodernphylogeneticstudies,Co leo chae ta les and Zygnematales are also characterized as sister groupsof landplants.Ultrastructuralstudiesrevealedcelldi vi sion due to a type of phragmoplast in Zygnematales that broughtthemtogetherwithcharophytic(Charales)andCo leo chae tes (Coleochaetales) algae, as well as with ter rest ri al plants (Mattox & Stewart 1974, PickettHeaps 1975. The fol lowing biochemical and molecular studies have found that Zygnematophyceae is one of the advanced groups of Strep to phytealgae,althoughnooneof theobtainedto po lo gies has been supported statistically.…”

“…Equally important, but rather essential for the evolution of Charophyte multicellularity andthefor ma tionof threedimensionalbody of plants ge ne ral ly, was the phragmoplast, which is a special adaptation in the form of ve siclesandmic ro tu bulesformedduringcyto ki nesis (PickettHeaps 1975). This process of inte rac tionbet weencellswasfoundinZyg ne ma ta les, Coleochaetales, Charales, and ter rest rialplants(Marchant&PickettHeaps1973).It is assumed that the emergence of phragmoplast con tributedtotheformationof twoorthree di men sionalorganisms'aggregatesof cellsdu ring their division, with further development of the integrated plant's thallome (Hageman 1999,PickettHeapsetal.1999.…”