Gaining or cutting SLAC: the evolution of plant guard cell signalling pathways

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.