Extensive embryonic patterning without cellular differentiation primes the plant epidermis for efficient post-embryonic stomatal activities

Plant leaves feature epidermal stomata that are organized in stereotyped patterns. How does the pattern originate? We provide transcriptomic, imaging, and genetic evidence that Arabidopsis embryos engage known stomatal fate and patterning factors to create regularly spaced stomatal precursor cells. Analysis of embryos from 36 plant species indicates that this trait is widespread among angiosperms. Embryonic sto-matal patterning in Arabidopsis is established in three stages: first, broad SPEECHLESS (SPCH) expression; second, coalescence of SPCH and its targets into discrete domains; and third, one round of asymmetric di-vision to create stomatal precursors. Lineage progression is then halted until after germination. We show that the embryonic stomatal pattern enables fast stomatal differentiation and photosynthetic activity upon germi-nation, but it also guides the formation of additional stomata as the leaf expands. In addition, key stomatal regulators are prevented from driving the fate transitions they can induce after germination, identifying stage-specific layers of regulation that control lineage progression during embryogenesis.

Automated summary

Plant leaves have organized epidermal stomata in stereotyped patterns. Arabidopsis embryos use known stomatal fate and patterning factors to create regularly spaced stomatal precursors. The embryonic stomatal pattern enables fast stomatal differentiation and guides the formation of additional stomata as the leaf expands. The regulation of stomatal regulators is stage-specific during embryogenesis.