Specialized Zones of Development in Roots: View from the Cellular Level

Recently, Ishikawa and Evans (1995) focused attention on the immediately postmitotic growth zone of plant roots and indicated its importance in root growth in response to interna1 and externa1 factors. This previously unrecognized region of the root, intercalated between the apical meristem and the zone of rapid cell elongation, was originally discovered as the result of a morphometric analysis of the breadthlength ratios of cells along the length of the maize root (BaluSka et al., 1990). The analysis indicated that as cells are displaced away from the root apex, their growth is adjusted in such a way that, in the immediate postmitotic region, approximately isodiametric (cuboidal) cellular shapes are obtained. Thus, the term "postmitotic 'isodiametric' growth" (or PIG) was coined for this region. In the cortex of maize primary roots the PIG zone was about 450 pm; in cultured tomato roots its length was about 380 pm. The length of this region thus represents about 5.5% of the entire growth zone. Subsequent studies confirmed the uniqueness of the cells located in the PIG zone, not only from a morphometrical point of view, but also on account of their specific cytological and physiological properties (Barlow et al., 1991; BaluSka et al., l992,1994,1996a, 1996c; Ishikawa and Evans, 1992, 1993, 1995). From a cellular point of view, the root tip has (a) a zone of cell division, a zone of more-or-less isotropic cell growth in which the cells both elongate and increase in width at similar rates; and (b) a zone of elongation in which cell growth is distinctly anisotropic and the rate of elongation is much greater than in the PIG zone. In cell-based terminology, therefore, the term "zone of cell elongation" should be reserved for root cells that grow in this strictly polar fashion. Significantly, our morphometric studies at the cellular leve1 showed that an abrupt decline of cellular widening coincided precisely with a prominent increase in the rate of cell lengthening, and this occurred at the base of the PIG region (BaluSka et al., 1990, 1994; Barlow et al., 1991). This occurrence provided the first hint that the newly formed postmitotic cells of the root may undergo some kind of preparatory phase wherein they adjust or reorganize their growth from the formerly slow, mitotic mode of growth to a rapid mode of elongation. Rapid cell elongation in roots is based in part on an extensive uptake of solutes coupled with the formation of a prominent vacuolar compartment. These events accelerate cell expansion, which is channeled with the aid of specific alignments of both the cortical microtubules (CMTs) in the cytoplasm and the cellulose microfibrils in the cell wall, into strictly anisotropic cell enlargement. A significant reorganization of the metabolic machinery is required to achieve this new mode of cell growth. For example, cells of maize root apices increase their volume approximately 10-fold in the 13 h during which they migrate through the elongation region, whereas in the meristem cell volume may only double during this period (BaluSka et al., 1996~). Once the rapid acceleration of cell growth has been triggered, it must be supported by a robust synthetic machinery that is obviously not yet operational in cells that are just ceasing their meristematic phase of development. If it were otherwise, root cells would commence their rapid elongation simultaneously with the termination of mitotic division. Not a11 cells of the root cease to divide at the same distance from the root tip, and it was recently found that the proximal limit of the meristem fluctuates in a rhythmic manner in accordance with a programmed pattern of transverse cell division within its constituent cell files (Liick et al., 1996). It is probably advantageous, therefore, for the early postmitotic root cells to enter a critica1 preparatory phase, located in a special transition zone behind the meristem, where they acquire the ability to embark on rapid elongation. Moreover, some supracellular organizing process within this transition zone may ensure the simultaneous commencement of the rapid elongation phase in cells of different tissues (epidermis, cortex, stele, etc.) at a particular distance from the root tip. Root-generated electric fields, for example, may be one way of defining the conditions required for a coordinated program of rapid elongation after cells have completed their preparatory phase within the transition zone. Also, within this zone cells develop the necessary synthetic machinery for the biogenesis of new tonoplast and plasma membranes, cell-wall components, new enzymatic complexes, and cytoplasmic structures that support such rapid growth. Aside from the basic synthetic machinery for cell growth, individual elements of the cytoskeleton can also be expected to alter their intracellular distribution from those configurations that support mitotic cell growth and division to arrangements that enable rapid cell elongation. In cells of the postmitotic transition zone, the CMTs change from loosely organized transverse arrays to an exclusively transverse orientation with respect to the root axis; the latter orientation is often accompanied by the appearance of