Regulation of hair cell and stomatal size by a hair-cell specific peroxidase in the grassBrachypodium distachyon

Abstract

The leaf epidermis is the outermost cell layer forming the interface between plants and the atmosphere that must both provide a robust barrier against (a)biotic stressors and facilitate carbon dioxide uptake and leaf transpiration1. To achieve these opposing requirements, the plant epidermis developed a wide range of specialized cell types such as stomata and hair cells. While factors forming these individual cell types are known2–5, it is poorly understood how their number and size is coordinated. Here, we identified a role forBdPRX76/BdPOX, a class III peroxidase, in regulating hair cell and stomatal size in the model grassBrachypodium distachyon. Inbdpoxmutants prickle hair cells were smaller and stomata were longer. Because stomatal density remained unchanged, the negative correlation between stomatal size and density was disrupted inbdpoxand resulted in higher stomatal conductance and lower intrinsic water-use efficiency.BdPOXwas exclusively expressed in hair cells suggesting thatBdPOXcell-autonomously promotes hair cell size and indirectly restricts stomatal length. Cell wall autofluorescence and lignin stainings indicated a role for BdPOX in lignification or crosslinking of related phenolic compounds at the hair cell base. Ectopic expression ofBdPOXin the stomatal lineage increased phenolic autofluorescence in guard cell walls and restricted stomatal elongation inbdpox. Together, we highlight a developmental interplay between hair cells and stomata that optimizes epidermal functionality. We propose that cell-type-specific changes disrupt this interplay and lead to compensatory developmental defects in other epidermal cell types.