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

Abstract

The evolution of adjustable plant pores (stomata), enabling CO2 acquisition in cuticle wax-sealed tissues was one of the most significant events in the development of life on land. But how did the guard cell signalling pathways that regulate stomatal movements evolve? We investigate this through comparison of fern and angiosperm guard cell transcriptomes. We find that these divergent plant groups share expression of similar genes in guard cells including biosynthesis and signalling genes for the drought stress hormone abscisic acid (ABA). However, despite conserved expression in guard cells, S-type anion channels from the SLAC/SLAH family - known for ABA-mediated stomatal closure in angiosperms - are not activated by the same pathways in ferns, highlighting likely differences in functionality. Examination of other land plant channels revealed a complex evolutionary history, featuring multiple gains or losses of SLAC activation mechanisms, as these channels were recruited to a role in stomatal closure. Taken together, the guard cells of flowering and non-flowering plants share similar core features, but also show lineage-specific and ecological niche-related adaptations, likely underlying differences in behaviour.