Unstable Phase Response Curves Shown by Spatiotemporal Patterns in the Plant Root Circadian Clock

Abstract

Phase response curves (PRCs) play important roles in the entrainment of periodic environmental cycles. Measuring the PRC is necessary to elucidate the relationship between environmental cues and the circadian clock. Conversely, the PRCs of plant circadian clocks are unstable due to multiple factors such as biotic/abiotic noise, individual differences, changes in amplitude, growth stage, and organ/tissue specificity. However, evaluating the effect of each factor is important because PRCs are commonly obtained by determining the response of many individuals, which include different amplitude states and organs. The plant root circadian clock spontaneously generates a spatiotemporal pattern called a stripe pattern, whereby all phases of the circadian rhythm exist within an individual root. Therefore, stimulating a plant root expressing this pattern enables phase responses at all phases to be measured using an individual root. In this study, we measured PRCs for thermal stimuli using this spatiotemporal pattern method and found that the PRC changed asymmetrically with positive and negative temperature stimuli. Individual differences were observed for weak but not for strong temperature stimuli. The root PRC changed depending on the amplitude of the circadian rhythm. The PRC in the young root near the hypocotyl was more sensitive than those in older roots or near the tip. Simulation with a phase oscillator model revealed the effect of measurement and internal noises on the PRC. These results indicate that instability in the entrainment of the plant circadian clock involves multiple factors, each having different characteristics. These results may help us understand how plant circadian clocks adapt to unstable environments and how plant circadian clocks with different characteristics, such as organ, age, and amplitude, are integrated within individuals.