Molecular control of stomatal development

Abstract

Plants have evolved developmental plasticity which allows the up- or down-regulation of photosynthetic and water loss capacities as new leaves emerge. This developmental plasticity enables plants to maximise fitness and to survive under differing environments. Stomata play a pivotal role in this adaptive process. These microscopic pores in the epidermis of leaves control gas exchange between the plant and its surrounding environment. Stomatal development involves regulated cell fate decisions that ensure optimal stomatal density and spacing, enabling efficient gas exchange. The cellular patterning process is regulated by a complex signalling pathway involving extracellular ligand-receptor interactions, which, in turn, modulate the activity of three master transcription factors essential for the formation of stomata. Here, we review the current understanding of the biochemical interactions between the epidermal patterning factor ligands and the ERECTA family of leucine-rich repeat receptor kinases. We discuss how this leads to activation of a kinase cascade, regulation of the bHLH transcription factor SPEECHLESS and its relatives, and ultimately alters stomatal production.

Keywords: guard cell; peptide ligand; plant biology; receptor kinase; transcription factors.

Figure 1.. Cells of the stomatal lineage.

(A) Vectorised confocal image of a young developing Arabidopsis abaxial leaf epidermis. This representative epidermis contains cells expressing each of the three bHLH transcription factors that control stomatal development. MMCs and meristemoids which contain SPCH are colored in green (B), while GMCs are in blue and contain MUTE (C). Newly formed and maturing guard cells are indicated by purple and express FAMA (D). Together with the pavement (white) and stomatal lineage ground cells (white), this forms the progression of protodermal cells through the stomatal lineage. (E) Cartoon to illustrate the controlled cell divisions and cell fate transitions that regulate stomatal development in the Arabidopsis early leaf epidermis.

Figure 2.. Receptor and ligand interactions govern SPCH and stomatal development.

Diagram of ligand–receptor interactions that regulate SPEECHLESS (SPCH) through phosphorylation of serine and threonine residues in the N-terminus and MAPK target domain (MPKTD). The binding of EPF1/2 ligand by the ERf/TMM/SERK receptor complex activates an MPK cascade that ultimately results in the negative regulation of SPCH through phosphorylation of the MPKTD which restricts stomatal development. STOMAGEN competes with EPF1/2 for the binding sites of the Erf/TMM/SERK complex to positively regulate stomatal development. In some tissues, brassinosteroids activate BIN2 through a BRI1/SERK complex which leads to negative regulation of YDA and SPCH. In the stem/hypocotyl, TMM acts to modulate the activation of the MPK cascade by reducing the affinity of the ERf for CHALLAH. Phosphorylation sites confirmed using in vitro or in vivo techniques are shown in bold. Sites that are regulated by BIN2 and the MPK cascade are indicated by asterisks.