A Circadian Clock- and PIF4-Mediated Double Coincidence Mechanism is Implicated in the Thermosensitive Photoperiodic Control of Plant Architectures in Arabidopsis thaliana

In Arabidopsis thaliana, the circadian clock regulates diurnal and photoperiodic plant growth including the elongation of hypocotyls in a time-of-day-specific and short-day (SD)-specific manner. The clock-controlled PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) encoding a basic helix-loop-helix (bHLH) transcription factor plays crucial roles in this regulation. PIF4 is transcribed precociously at the end of the night in SDs, under which conditions the protein product is stably accumulated, while PIF4 is expressed exclusively during the daytime in long days (LDs), under which conditions the protein product is degraded by light-activated phytochrome B. The dawn- and SD-specific elongation of hypocotyls is best explained by the coincident accumulation of the active PIF4 protein during the night-time before dawn specifically in SDs. However, this coincidence model was challenged with the recent finding that the elongation of hypocotyls is markedly promoted at high growth temperature (i.e. 28 degrees C) even under LDs in a PIF4-dependent manner. Here, we reconciled these apparently conflicting facts by showing that the transcription of PIF4 occurs precociously at the end of the night-time at 28 degrees C in LDs, similarly to in SDs. Both the events resulted in the same consequence, i.e. that a set of PIF4 target genes (ATHB2, GH3.5, IAA19, IAA29, BRox2, GAI, ACS8 and CKX5) was induced accordingly in a time-of-day-specific manner. Taken together, we propose an extended double coincidence mechanism, by which the two environmental cues (i.e. photoperiods and temperatures), both of which vary on a season to season basis, are integrated into the same clock- and PIF4-mediated output pathway and regulate a hormone signaling network to fit plant architectures properly to domestic habitats.