ERECTA signaling controls the timing of Arabidopsis Guard Cell maturation at the embryonic leaf tip

While cell identities are established early during embryogenesis, these cells remain immature until germination, and the mechanisms enforcing this developmental pause are poorly understood. Embryonic stomatal cells provide a model to study this pause as the stomatal transcription factor FAMA, normally sufficient for Guard Cell maturation in seedlings, can not drive maturation in the Arabidopsis embryo. Here we show that FAMA’s ability to drive maturation depends on leaf polarity and adaxial stomatal cells can progress further in their lineage. We next find that ERECTA-family receptor signaling, which controls stomatal patterning, also suppresses embryonic stomatal maturation. In er erl1 erl2 mutants, cell pairs at the cotyledon tip acquire characteristics of maturing guard cells: cell wall reinforcement, pore-associated thickening, and expression of late lineage markers as identified by whole embryo transcriptomics. This precocious maturation however remains incomplete: many GC markers remain absent, and cells lack an open pore and mature vacuoles. Genetic analysis shows that partial maturation requires but is not limited by low levels of FAMA. Restriction of maturation to the cotyledon tip correlates with locally elevated ERECTA-family receptor abundance, while high auxin appears dispensable for this. Finally, we show that EPFL-ER signaling mediates leaf tip Guard Cell size postembryonically as well. Altogether, we identify ERECTA signaling as a local brake on embryonic stomatal cell maturation, discovering another way to push precocious stomatal cell maturation that results in a complex, partially mature cell state that provide insights into the limitations on cell embryonic cell maturation.