A Per-ARNT-Sim-Like Sensor Domain Uniquely Regulates the Activity of the Homeodomain Leucine Zipper Transcription Factor REVOLUTA in Arabidopsis

Class III homeodomain leucine zipper (HD-ZIP III) transcription factors regulate critical developmental programs in plants; these include leaf polarity, polarity along the shoot-root axis, and stem cell specification and proliferation. One of the defining features of HD-ZIP III proteins is the presence of a Per-ARNT-Sim-like (PAS-like) MEKHLA domain at the C terminus. PAS-like domains are known to respond to a variety of chemical and physical stimuli. Here, we provide evidence that the MEKHLA domain acts as a negative regulator of Arabidopsis thaliana HD-ZIP III REVOLUTA activity. Based on experiments in yeast and plants, we propose a model in which the MEKHLA domain inhibits dimerization through a sequence-independent steric masking mechanism. This inhibition is relieved in response to a cellular signal that requires the C terminus of the MEKHLA domain for its perception. Overexpression experiments suggest that this signal is unequally distributed and/or sensed in the plant. Our data show that the function of the REVOLUTA MEKHLA domain differs among other HD-ZIP III family members; this difference may explain the genetic differences that have been observed among family members. This finding, combined with our phylogenetic analysis, suggests that REVOLUTA is the latest type of HD-ZIP III protein to have evolved in land plants.