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Summary: The evolution of adjustable stomatal pores, enabling CO2 acquisition, was one of the most significant events in the development of life on land. Here, we investigate how the guard cell signalling pathways that regulate stomatal movements evolved.We compare fern and angiosperm guard cell transcriptomes and physiological responses, and examine the functionality of ion channels from diverse plant species.We find that, despite conserved expression in guard cells, fern anion channels from the SLAC/SLAH family are not activated by the same abscisic acid (ABA) pathways that provoke stomatal closure in angiosperms. Accordingly, we find an insensitivity of fern stomata to ABA. Moreover, our analysis points to a complex evolutionary history, featuring multiple gains and/or losses of SLAC activation mechanisms, as these channels were recruited to a role in stomatal closure.Our results show that the guard cells of flowering and nonflowering plants share similar core features, with lineage‐specific and ecological niche‐related adaptations, likely underlying differences in behaviour. [ABSTRACT FROM AUTHOR]

Summary: Recent studies have revealed that some responses of fern stomata to environmental signals differ from those of their relatives in seed plants. However, it is unknown whether the biophysical properties of guard cells differ fundamentally between species of both clades. Intracellular micro‐electrodes and the fluorescent Ca2+ reporter FURA2 were used to study voltage‐dependent cation channels and Ca2+ signals in guard cells of the ferns Polypodium vulgare and Asplenium scolopendrium. Voltage clamp experiments with fern guard cells revealed similar properties of voltage‐dependent K+ channels as found in seed plants. However, fluorescent dyes moved within the fern stomata, from one guard cell to the other, which does not occur in most seed plants. Despite the presence of plasmodesmata, which interconnect fern guard cells, Ca2+ signals could be elicited in each of the cells individually. Based on the common properties of voltage‐dependent channels in ferns and seed plants, it is likely that these key transport proteins are conserved in vascular plants. However, the symplastic connections between fern guard cells in mature stomata indicate that the biophysical mechanisms that control stomatal movements differ between ferns and seed plants. [ABSTRACT FROM AUTHOR]