Early evolutionary acquisition of stomatal control and development gene signalling networks

•Core CO2, light, and ABA stomatal response genes in seed plants are expressed in stomata-bearing moss sporophytes.•These tool kits enable the stomata of bryophytes and some lycophytes to respond to environmental (CO2 and light) and endogenous (abscisic acid, ABA) signals.•Key genes regulating stomatal development in seed plants are expressed in stomata-bearing moss sporophytes.•Stomatal responses probably originated early in land plant evolution, in the ancestor of mosses.

Fossil stomata of early vascular land plants date back over 418 million years and exhibit properties suggesting that they were operational, including differentially thickened guard cells and sub-stomatal chambers. Molecular studies on basal land plant groups (bryophytes and lycophytes) provide insight into the core genes involved in sensing and translating changes in the drought hormone abscisic acid (ABA), light and concentration of CO2 into changes in stomatal aperture. These studies indicate that early land plants probably possessed the genetic tool kits for stomata to actively respond to environmental/endogenous cues. With these ancestral molecular genetic tool kits in place, stomatal regulation of plant carbon and water relations may have became progressively more effective as hydraulic systems evolved in seed plant lineages. Gene expression and cross-species gene complementation studies suggest that the pathway regulating stomatal fate may also have been conserved across land plant evolution. This emerging area offers a fascinating glimpse into the potential genetic tool kits used by the earliest vascular land plants to build and operate the stomata preserved in the fossil record.