Continuous dynamic adjustment of the plant circadian oscillator

Abstract

The clockwork of plant circadian oscillators has been resolved through investigations in Arabidopsis thaliana. The circadian oscillator is an important regulator of much of plant physiology, though many of the mechanisms are unclear. New findings demonstrate that the oscillator adjusts phase and period in response to abiotic and biotic signals, providing insight in to how the plant circadian oscillator integrates with the biology of the cell and entrains to light, dark and temperature cycles. We propose that the plant circadian oscillator is dynamically plastic, in constant adjustment, rather than being an isolated clock impervious to cellular events.

Fig. 1

Circadian oscillators are entrained timekeepers. a The circadian oscillator contains a network of transcriptional regulators. The components regulate each other in a temporal series, indicated by the flow of the arrows. The extensive regulation between components has been omitted for clarity; for details, see references in the text. The components can be grouped functionally as MYB-like repressors (cyan), MYB-like activators (red), pseudo response regulators (yellow), nocturnal regulators (dark grey) and proteins involved in protein stability (light grey). b The circadian oscillator is often conceptualised as a mechanical clock, with “cogs” made up of the functional groups of transcriptional regulators, “hands” that provide a read-out of time and the clock is set to a new time at light (yellow box) and dark (black box) interfaces (red dotted line). c Entrainment is thought to occur through non-parametric changes that jump from one point in the cycle to another in an almost instantaneous change in state of the oscillator and parametric changes that require acceleration or deceleration of the oscillator

Fig. 2

The loosely coupled nature of the oscillator is demonstrated by the plasticity of peak time of expression of the components of the circadian oscillator. Peak of oscillator transcript abundance is plotted against time since dawn (h). Upper plot: a photoperiod of 6 h light (yellow box) and 18 h dark (grey box); lower plot:18 h light 6 h dark. The time of the peaks shifts between the photoperiods relative to the external photoperiod and relative to each other. Distance from the time line on the y axis is for plotting clarity and conveys no meaning. The data were obtained from Table S2

Fig. 3

Entrainment might involve transient changes in the velocity of an oscillator. We can conceptualise the problem of entrainment as setting the hands of a travel clock when moving between time zones. In the cartoon, we can see that if we move the time zones and readjust the hands of the clock to a new time zone, there is a temporary speeding up or slowing down of the movement of the hands to adjust to the new time zone, before the clock returns to its fixed velocity

Fig. 4

Dynamic phase adjustment of circadian oscillator through regulation of individual components. Entrainment occurs through signalling to individual components based on their temporal availability. At dawn, light-regulated transcription factors, including PIF3, regulate CCA1 expression, sugars regulate bZIP63 to modulate PRR7 expression to establish a metabolic dawn^, and dusk is sensed through ZTL-mediated degradation of TOC1 protein in the dark. Each entrainment event is semi-discrete, can have potential for downstream components, but might also be temporally restricted due to subsequent inputs. The sequential nature is akin to a signalling pathway rather than the resetting of an entire clock mechanism. The wave form for these components in a 12-h light and 12-h dark cycle normalised to peak height indicates the times of potential regulation. Red (CCA1), black (PRR7) and blue (TOC1). Dashed lines are mRNA, solid line is the protein. Data for the plots were obtained from digitised data sets of CCA1 mRNA, PRR7 mRNA and protein, and TOC1 mRNA and protein. This collection does not contain light/dark cycle data for CCA1 protein

Fig. 5

Dynamic plasticity of circadian rhythms might contribute to carbon homoeostasis in Arabidopsis. a There are diel changes in the transient starch pool stored in the chloroplasts, with the rate of accumulation and loss being near linear and adjusting to the photoperiod. b It has been proposed that the circadian clock generates an output that is a measure of time until dawn (T). This interacts with a measure of the size of the starch granule (S) to set a constant rate of starch degradation until dawn. In this model, the rate of degradation is calculated individually in the 100s of chloroplasts in a mesophyll cell. This model class assumes that starch pool size is regulated. c Another proposal is that the circadian clock regulates the starch degradation activity (β), such that it peaks near dawn. Sugars released from starch degradation in the chloroplast feedback to regulate the circadian oscillator in the nucleus by affecting the pool of available C. The circadian oscillator is dynamically adjusted to maintain available C homoeostasis in a form of retrograde signalling. d In the morning, a rising rate of change of sugars promotes phase advance (red), which will have the effect of reducing β at any particular time point. A phase delay in the morning will increase β at any time point, increasing starch degrading activity (not shown). Phase delays by sugars at night will have the effect of reducing β