Circadian clock-regulated physiological outputs: dynamic responses in nature

Abstract

The plant circadian clock is involved in the regulation of numerous processes. It serves as a timekeeper to ensure that the onset of key developmental events coincides with the appropriate conditions. Although internal oscillating clock mechanisms likely evolved in response to the earth's predictable day and night cycles, organisms must integrate a range of external and internal cues to adjust development and physiology. Here we introduce three different clock outputs to illustrate the complexity of clock control. Clock-regulated diurnal growth is altered by environmental stimuli. The complexity of the photoperiodic flowering pathway highlights numerous nodes through which plants may integrate information to modulate the timing of flowering. Comparative analyses among ecotypes that differ in flowering response reveal additional environmental cues and molecular processes that have developed to influence flowering. We also explore the process of cold acclimation, where circadian inputs, light quality, and stress responses converge to improve freezing tolerance in anticipation of colder temperatures.

Fig. 1. Circadian clock-mediated diurnal hypocotyl growth

(A, B) Arabidopsis hypocotyl growth for 4 to 5-day-old seedlings, before their cotyledons are fully expanded, is regulated by different inputs at different parts of the day. (A) Hypocotyl growth rate is most affected by light intensity at dusk. (B) Carbon source availability most affects the growth rate at dawn (dusk and dawn are indicated by open arrowheads). The graphs were modified from [7]. (C) The circadian clock coordinates various pathways involved in diurnal growth regulation. These pathways include phytochrome, sucrose and GA signaling, and the components (ELF3, ELF4, and LUX) of the evening complex, ultimately resulting in transcriptional or post-translational regulation of PIF4 and PIF5. Higher sucrose levels reduce the degradation rate of PIF5 resulting in an enlarged morning response to growth. PHYB signals keep PIF levels low under light. The evening complex represses the expression of PIF4 and PIF5 at dusk. Higher amounts of GA-GID1 complex around dawn induces degradation of DELLA proteins, which prevent PIF4 (and possibly PIF5) from binding to target DNA. PIF4/PIF5 mRNA profile is shown by a pink line. Coordinated regulation by the clock contributes to temporally confined growth that occurs at dawn and dusk through convergence of light, hormone, and metabolic signaling.

Fig. 2. Circadian clock regulation of the cold acclimation pathway in Arabidopsis

(A) Inputs from the circadian clock, light signaling, and temperature activate COR genes through the CBF transcriptional activators, which induce the process of cold acclimation in Arabidopsis. In the diagram, colored lines are given to help distinguish interactions between different components. Cold temperatures induce CBF expression through CCA1 alternative splicing. The accumulation of the functional CCA1α splice variant in low temperatures increases CBF expression. Competition for the non-functional CCA1β variant at higher temperatures attenuates the cold response. TOC1 and PRR5 directly repress CBF expression in the evening and PRR7 and PRR9 likely act in a similar manner. Changes in the red/far-red light ratio are sensed through PHYB and PHYD, which in low red/far-red conditions drive transcriptional activation of CBF genes through PIF4 and PIF7. TOC1 protein binds to the PIF4 promoter and may physically interact with PIF7 protein [70, 74]. Through these mechanisms, the circadian clock, temperature, and light inputs mediate and amplify environmental signals to induce cold acclimation. (B) Relative abundance of clock component proteins at different times of the day dictates temporal CBF expression. In the morning, CCA1 activates CBFs, which in turn activate COR downstream genes. In the evening, TOC1 and PRR5 repress CBF expression. Schematic protein and mRNA levels are drawn from data in which plants were grown in continuous light conditions [64, 76, 77].