Circadian Clock- and PIF4-Controlled Plant Growth: A Coincidence Mechanism Directly Integrates a Hormone Signaling Network into the Photoperiodic Control of Plant Architectures in Arabidopsis thaliana

The plant circadian clock generates rhythms with a period close to 24 h, and it controls a wide variety of physiological and developmental events, enabling plants to adapt to ever-changing environmental light conditions. In Arabidopsis thaliana, the clock regulates the diurnal and photoperiodic plant growth including the elongation of hypocotyls and petioles in a time-of-day-specific and short-day (SD)-specific manner. In this mechanism, the clock-regulated PHYTOCHROME-INTERACTING FACTOR 4 gene encoding a basic helix-loop-helix transcription factor, together with phytochromes (mainly phyB), plays crucial roles. This diurnal and photoperiodic control of plant growth is best explained by the accumulation of the PIF4 protein at the end of the night-time specifically under SDs, due to coincidence between the internal (circadian rhythm) and external (photoperiod) cues. In this model, however, the PIF4-controlled downstream factors are not fully identified, although it has been generally proposed that the auxin-mediated signal transduction is crucially implicated. Here, we identified a set of hormone-associated genes as the specific PIF4 targets implicated in the photoperiodic control of plant growth. They include not only auxin-associated genes (GH3.5, IAA19 and IAA29), but also genes associated with other growth-regulating hormones such as brassinosteroids (BR6ox2), gibberellic acids (GAI), ethylene (ACS8) and cytokinin (CKX5). The dawn- and SD-specific expression profiles of these genes are modified in a set of phyB and clock mutants, both of which compromise the coincidence mechanism. The results of this study suggest that the circadian clock orchestrates a variety of hormone signaling pathways to regulate the photoperiod-dependent morphogenesis in A. thaliana.