Are dumbbell stomata unique? Diversified developmental trajectories in sedges and grasses result in partially convergent stomata

Abstract

Dumbbell-shaped stomata in grasses represent an evolutionary novelty, as their distinctive guard cell morphology is absent from most plant lineages. Stomata exhibit two major morphological forms: the kidney-shaped type found in most plants, and the dumbbell-shaped type that evolved in grasses. Dumbbell-like forms occur in sedges (Cyperaceae), providing an opportunity to examine how changes in developmental trajectories contribute to morphological evolution. By integrating analyses of cellulose microfibril organization, guard cell length to width ratio, and nuclear morphology, we demonstrate partial convergence between sedge and grass stomatal development. Specifically, cellulose microfibril organization in sedges represents an intermediate developmental state between kidney-shaped stomata and the grass dumbbell-shaped stomata. We further document differences in nuclear architecture: in contrast to kidney-shaped stomata, which have rounded nuclei in central guard cell regions, sedge nuclei are partially elongated and localize within bulbous regions, whereas grass nuclei exhibit fully elongated shapes along the cell axis. Notably, we identified secondary plasmodesmata between guard cells in one sedge species, suggesting a convergent route to symplastic communication achieved through secondary plasmodesmata formation rather than the incomplete cytokinesis characteristic of grasses. Together, these findings reveal convergent developmental solutions underlying similar stomatal morphologies.