Analysis of cell division patterns in the Arabidopsis shoot apical meristem

Abstract

The stereotypic pattern of cell shapes in the Arabidopsis shoot apical meristem (SAM) suggests that strict rules govern the placement of new walls during cell division. When a cell in the SAM divides, a new wall is built that connects existing walls and divides the cytoplasm of the daughter cells. Because features that are determined by the placement of new walls such as cell size, shape, and number of neighbors are highly regular, rules must exist for maintaining such order. Here we present a quantitative model of these rules that incorporates different observed features of cell division. Each feature is incorporated into a "potential function" that contributes a single term to a total analog of potential energy. New cell walls are predicted to occur at locations where the potential function is minimized. Quantitative terms that represent the well-known historical rules of plant cell division, such as those given by Hofmeister, Errera, and Sachs are developed and evaluated against observed cell divisions in the epidermal layer (L1) of Arabidopsis thaliana SAM. The method is general enough to allow additional terms for nongeometric properties such as internal concentration gradients and mechanical tensile forces.cell division | computer modeling | live imaging | Arabidopsis T he Arabidopsis shoot apical meristem (SAM) is a structure at the tip of the shoot that is responsible for generating almost all of the above-ground tissue of the plant (1). Its epidermal and subepidermal cells are organized into layers with very few cells moving between layers (2, 3). When these cells expand they do so laterally, pushing other cells toward the periphery of the meristem. Division in these cells is anticlinal such that each layer remains one cell thick. The underlying mechanism determining the location of new cell walls is unknown but the qualitative properties of meristematic cell division are well documented (4-8). Perhaps the best known summary is Errera's rule, derived following observations of soap bubble formation. In the modern interpretation, the plane of division corresponds to the shortest path that will halve the mother cell. Errera, in fact, wrote that the wall would be a surface "mit constanter mittlerer Krümmung (= Minimalfläche) [with constant mean curvature (= minimal area)]" (4). Because this does not specify a location for the new cell wall, more recent authors have added to this that the mother cell divides evenly (9, 10). With this modification, Errera's rule is easily quantifiable.A second observation is Hofmeister's rule: New cell walls usually form in a plane normal to the principal axis of cell elongation (5). This rule is more difficult to quantify, because the principal axis of cell elongation is often confused with the direction of growth. Cells are asymmetrical and hence a principal direction of cell elongation can easily be calculated (e.g., the principal axis of inertia or principal component of a segmentation). The assumption is often made that because the cell is more elongated in one direction...

Cell-size dependent progression of the cell cycle creates homeostasis and flexibility of plant cell size

“…Consistent with previous studies3835, we found that ∼60% of divisions produced daughters with >5 μm 2 difference in outer cell surface area at birth, equivalent to inheriting on average >54% of the parental area (Supplementary Fig. 2a,b).…”

“…Analysis of cell growth rates in the SAM suggests cell size control is required35 and indeed most models of plant tissue growth assume that cell division is triggered when cells reach a defined cell size36373839. However no cell-sizing mechanism has been proposed or identified for plant cells, and little is known about how cells behave when variation in cell size arises, or how changes in cell size are regulated during development.…”

Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche

“…The mean interdivision time was 21-31 h among SAMs, which is similar to a previous time-lapse imaging study of SAMs not grown on NPA (15). Our data confirmed reported distributions of L1 cell neighbor numbers, outer periclinal wall areas, and the linear relation (Lewis' law) between number of neighbors and outer periclinal wall area (32)(33)(34)(35) (Fig. 1E and SI Appendix, Figs.…”

Cell division plane orientation based on tensile stress inArabidopsis thaliana

“…These geometric rules were also tested in the Arabidopsis shoot apical meristem (SAM), a dome-shaped group of dividing cells that generates every aerial organ. Although Errera's rule described the highest percentage of divisions, neither Hofmeister's, nor Errera's, nor Sachs' rules fully described all of the divisions at the SAM (7).…”