Circadian entrainment in Arabidopsis

Abstract

Circadian clocks coordinate physiology and development as an adaption to the oscillating day/night cycle caused by the rotation of Earth on its axis and the changing length of day and night away from the equator caused by orbiting the sun. Circadian clocks confer advantages by entraining to rhythmic environmental cycles to ensure that internal events within the plant occur at the correct time with respect to the cyclic external environment. Advances in determining the structure of circadian oscillators and the pathways that allow them to respond to light, temperature, and metabolic signals have begun to provide a mechanistic insight to the process of entrainment in Arabidopsis (Arabidopsis thaliana). We describe the concepts of entrainment and how it occurs. It is likely that a thorough mechanistic understanding of the genetic and physiological basis of circadian entrainment will provide opportunities for crop improvement.

Figure 1

Different approaches allow visualization and analysis of the effects of zeitgebers on circadian oscillators. A, PRCs plot the effect of a stimulus on circadian phase dependent on the time at which a pulse of stimulus is added in otherwise constant conditions. B, Data used to generate PRCs can be plotted as a PTC in which the phase before stimulation is plotted against the phase after stimulation. The angle of the slope indicates the strength of entrainment. C, Limit cycle analysis plots the relationship between variables in the oscillator (e.g. expression levels of oscillator genes) through time in 2D space (black). A stimulus (star) causes phase advance (blue) or delay (red) dependent upon the point in the cycle in which the stimulus is added. In this example, the stimulus that caused the phase advance (blue) initiates the reduction in state variable 1 earlier than would have occurred without perturbation, which is why the phase is advanced. Axes for the limit cycle are normalized arbitrary units.

Figure 2

Mechanisms of light entrainment of the Arabidopsis circadian oscillator. Simplified schematic diagram illustrating different mechanisms by which light might entrain the Arabidopsis circadian oscillator. The transcriptional oscillator is depicted in the bottom half of the figure with components grouped as previously described (Fogelmark and Troein, 2014). Pointed arrow heads represent activation, flat heads represent repression. The top half of the figure outlines examples of posttranslational regulation with components in circles being involved in this type of regulation. Blue background indicates the protein is involved in blue light regulation of the oscillator and red indicates association with red light signalling of the clock. Dashed oval surrounding components paired together indicates stabilization, red cross indicates that component is degraded by the direct or indirect action of its uncrossed neighbor. The figure is approximately organized by time of day going from dawn on the left (sun) to night on the right (crescent moon).

Figure 3

Simplified overview of potential temperature entrainment mechanisms. Schematic showing how cold (snowflake) and heat (sun) are transduced to the circadian clock. Circadian clock proteins are denoted by green ovals, components upregulated in the cold denoted by blue ovals, and components upregulated in the heat denoted by orange ovals. Dashed lines from CCA1 and LHY denote alternative splicing with CCA1α retaining the ability to bind to target DNA sequences and LHY-1R representing intron retaining splice variants that are targeted for nonsense-mediated decay (NMD). Pointed arrow heads represent activation, blunt arrow heads represent repression, and scissors represent proteasomal mediated degradation of proteins. Large red oval containing GI-ZTL-HSP90 represents complex where ZTL is unable to ubiquitinate PRR5 and TOC1. Gray oval labeled EC represents the EC where ELF3 is the target of degradation by the XBAT31–XBAT35–BBX18 complex but is stabilized by PhyB.

Figure 4

Entrainment of the Arabidopsis circadian oscillator by sugar schematic indicating how sugar can alter the expression of the core clock components CCA1 and LHY. Arrowheads represent activation, blunt heads represent repression, and dashed line represents possible interaction.