The Circadian Clock Regulates Auxin Signaling and Responses in Arabidopsis

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Abstract
The circadian clock plays a pervasive role in the temporal regulation of plant physiology, environmental responsiveness, and development. In contrast, the phytohormone auxin plays a similarly far-reaching role in the spatial regulation of plant growth and development. Went and Thimann noted 70 years ago that plant sensitivity to auxin varied according to the time of day, an observation that they could not explain. Here we present work that explains this puzzle, demonstrating that the circadian clock regulates auxin signal transduction. Using genome-wide transcriptional profiling, we found many auxin-induced genes are under clock regulation. We verified that endogenous auxin signaling is clock regulated with a luciferase-based assay. Exogenous auxin has only modest effects on the plant clock, but the clock controls plant sensitivity to applied auxin. Notably, we found both transcriptional and growth responses to exogenous auxin are gated by the clock. Thus the circadian clock regulates some, and perhaps all, auxin responses. Consequently, many aspects of plant physiology not previously thought to be under circadian control may show time-of-day–specific sensitivity, with likely important consequences for plant growth and environmental responses. Most higher organisms, including plants and animals, have developed a time-keeping mechanism that allows them to anticipate daily fluctuations of environmental parameters such as light and temperature. This circadian clock efficiently coordinates plant growth and metabolism with respect to time of day by producing self-sustained rhythms of gene expression with an approximately 24-h period. One of the major contributors in specifying spatial patterns of plant growth and development is auxin, a hormone essential for nearly all stages of plant development. Auxin also helps the plant orient itself properly in response to environmental cues such as light, gravity, and water. We have now found circadian-regulated expression of components from nearly every step in the auxin-signaling pathway, from synthesis to response. We demonstrate the relevance of this observation by showing that plants have differential sensitivity to auxin at different times of day: the clock controls plant sensitivity to auxin at both the level of transcription and stem growth. Our work demonstrates an intimate connection between the clock- and auxin-signaling pathways, and suggests that other auxin-regulated processes may also be under circadian control.