Stomatal Patterns in Embryophytes: Their Evolution, Ontogeny and Interpretation

Abstract

The history of study and nomenclature of stomatal concepts has not yet led to full elucidation of cell pattern significancefor higher plants. In this paper, a new ontogenetic system of classification is introduced that makes primary subdivision on the basis of the mode of division of the guard mother cell (GMC) with respect to the wall which cuts it from the meristemoid: diameristic, at right angles; parameristic, parallel to; and anomomeristic, without special orientation to the preceding wall. These are further subdivided on the basis of ontogeny and number of the surrounding cells. The biology of stomata is discussed as it relates to cell patterning, and fundamental ties are pointed out between stomatal configurations and epidermal ontogeny, especially with regard to whether development is rectate, proceeding in a wave from an intercalary or marginal meristem, or diffuse, proceeding with continued meristematic activity within the expanding tissue over a long period of time. The concept of perigenous stomata, those in which protodermal cells act directly as GMC's without prior division, is refuted. The primitive stoma of land plant sporophytes is interpreted to be the simplest type of diameristic, mesoperigenous stoma, in which a protodermal meristemoid divides transversely, cutting off a distal GMC which then divides longitudinally to produce the guard cells. This stoma is suggested as the progenitor type for the Angiospermae, and is the primitive type for at least the Monocotyledonae.

Out of the Mouths of Plants: The Molecular Basis of the Evolution and Diversity of Stomatal Development

“…Therefore, the diversity of stomata consists of variations on a theme: stomata are spaced at least one cell apart, but the specifics differ. Classic anatomical studies suggest that differences in stomatal patterning reflect the types, positions, and numbers of cell divisions that give rise to the stomatal complex (Esau, 1977;Payne, 1979). In this section, we describe stomatal development in other plant taxa and speculate regarding their possible alterations of regulatory mechanisms known in Arabidopsis.…”

“…In mosses and lycophytes ( Figures 1A and 1B), stomata develop through a simple process of a single asymmetric division followed by differentiation of a GMC, then GCs (Payne, 1979). We could speculate that the ancient function of SPCH-MUTE-FAMA family proteins may be to initiate the stomatal cell lineage and differentiate into GMC directly.…”

“…Since stomata evolved only once in the ancestor of the mosses (Raven, 2002), it is expected that plants that arose from different basal land plant lineages, such as P. patens, would also possess some if not all of the genes found to be essential for stomatal patterning and differentiation in Arabidopsis. Stomata in moss form through a single asymmetric cell division to produce a GMC, which will divide partially or completely to produce a single GC or a pair of GCs surrounding a pore (Payne, 1979). Congruent with this relatively simplified developmental sequence to mature GC formation, the moss P. patens does not have genes encoding SPCH or MUTE.…”

Origins and Evolution of Stomatal Development

“…Stomata are also a major site of pathogen entry and plant defense (Gudesblat et al, 2009). Despite their central role in so many processes, their origins and evolutionary history have long been a matter of considerable debate (Payne, 1979;Chater et al, 2011;Pressel et al, 2014;Franks and Britton-Harper, 2016;McAdam and Brodribb, 2016). Along with root-like structures, a waxy cuticle, and vasculature, stomata were a key innovation that enabled plants to conquer the land ( Fig.…”

Epidermal cell fate and patterning in leaves.

“…Satellite meristemoids also often divide asymmetrically one or more times through a series of oriented cell divisions, thus producing additional neighbor cells that further separate the two stomata ( Figure 5A). By contrast, the placement of the division that produces primary meristemoids is thought to be generally random in dicots (for exceptions, see Payne, 1979;Pappas et al, 1988). Moreover, so far as is known, the selection of the protodermal cells that are to become meristemoid mother cells also appears to be random (Sachs, 1994).…”