Stomatal development in the context of epidermal tissues

BACKGROUND: Stomata are adjustable pores on the surface of plant shoots for efficient gas exchange and water control. The presence of stomata is essential for plant growth and survival, and the evolution of stomata is considered as a key developmental innovation of the land plants, allowing colonization on land from aquatic environments some 450 million years ago. In the past two decades, molecular genetic studies using the model plant Arabidopsis thaliana identified key genes and signalling modules that regulate stomatal development: master regulatory transcription factors that orchestrate cell state transitions and peptide–receptor signal transduction pathways, which, together, enforce proper patterning of stomata within the epidermis. Studies in diverse plant species, ranging from bryophytes to angiosperm grasses, have begun to unravel the conservation and uniqueness of the core modules in stomatal development. SCOPE: Here, I review the mechanisms of stomatal development in the context of epidermal tissue patterning. First, I introduce the core regulatory mechanisms of stomatal patterning and differentiation in the model species A. thaliana. Subsequently, experimental evidence is presented supporting the idea that different cell types within the leaf epidermis, namely stomata, hydathodes pores, pavement cells and trichomes, either share developmental origins or mutually influence each other’s gene regulatory circuits during development. Emphasis is placed on extrinsic and intrinsic signals regulating the balance between stomata and pavement cells, specifically by controlling the fate of stomatal-lineage ground cells (SLGCs) to remain within the stomatal cell lineage or differentiate into pavement cells. Finally, I discuss the influence of intertissue layer communication between the epidermis and underlying mesophyll/vascular tissues on stomatal differentiation. Understanding the dynamic behaviours of stomatal precursor cells and their differentiation in the broader context of tissue and organ development may help design plants tailored for optimal growth and productivity in specific agricultural applications and a changing environment.