Symplastic guard cell connections buffer pressure fluctuations to promote stomatal function in grasses

Stomata regulate plant gas exchange via repeated turgor-driven changes of guard cell shape, thereby adjusting pore apertures. Grasses, which are among the most widespread plant families on the planet, are distinguished by their unique stomatal structure, which is proposed to have significantly contributed to their evolutionary and agricultural success. One component of their structure, which has received little attention, is the presence of a discontinuous adjoining cell wall of the guard cell pair. Here, we demonstrate the presence of these symplastic connections in a range of grasses and use finite element method simulations to assess hypotheses for their functional significance. Our results show that opening of the stomatal pore is maximal when the turgor pressure in dumbbell-shaped grass guard cells is equal, especially under the low pressure conditions that occur during the early phase of stomatal opening. By contrast, we demonstrate that turgor pressure differences have less effect on the opening of kidney-shaped guard cells, characteristic of the majority of land plants, where guard cell connections are rarely or not observed. Our data describe a functional mechanism based on cellular mechanics, which plausibly facilitated a major transition in plant evolution and crop development.