How plants tell the time

Abstract

Plants, like all eukaryotes and most prokaryotes, have evolved sophisticated mechanisms for anticipating predictable environmental changes that arise due to the rotation of the Earth on its axis. These mechanisms are collectively termed the circadian clock. Many aspects of plant physiology, metabolism and development are under circadian control and a large proportion of the transcriptome exhibits circadian regulation. In the present review, we describe the advances in determining the molecular nature of the circadian oscillator and propose an architecture of several interlocking negative-feedback loops. The adaptive advantages of circadian control, with particular reference to the regulation of metabolism, are also considered. We review the evidence for the presence of multiple circadian oscillator types located in within individual cells and in different tissues.

Figure 1. Schematic representation of circadian clock structures

(a) A model depicting division of the clock into an input pathway, a central oscillator and an output pathway. (b) An elaborated description of the clock, consisting of multiple core oscillators, gated input pathways and outputs which feed back into the central oscillator. Arrows are positive arms and perpendicular lines represent negative arms of the pathway.

Figure 2. Proposed structure of the CCA/LHY–TOC1 feedback loop

Light input, together with TOC1, induces the expression of CCA1 and LHY. CCA1 and LHY activate the expression of clock-controlled genes (CCGs, shown in mauve) and repress TOC1 expression [63] which in turn represses LHY/CCA1 expression. Light input is mediated by the CRYs and PHYs. Arrows represent positive regulatory steps, perpendicular lines indicate negative interactions. Genes are represented by rectangles and proteins as ovals.

Figure 3. Revised model of the LHY–TOC1 feedback loop [72,73]

Mathematical analysis indicates that the additional components X and Y are required in order to form a robust oscillator that matches the properties of the Arabidopsis clock. X is a gene that is required for the activation of LHY by TOC1. Y is a hypothetical gene that is activated by light and in turn activates TOC1. Y is repressed by both TOC1 and LHY. GI is a candidate for the identity of Y. X is currently unknown. Arrows represent positive regulatory steps, perpendicular lines indicate negative interactions. Genes are represented by rectangles and proteins as ovals.

Figure 4. Model of the Arabidopsis circadian clock

The model is based on recent analyses which indicate that multiple feedback loops exist within the Arabidopsis clock. The CCA1–LHY–TOC1–GI–X feedback loop is outlined in [72,73], the PRR loop in [62,25], and the ELF4 loop in [79]. PHYs, CRYs and ELF3 are under transcriptional control by the circadian clock, so essentially represent additional loops [48,53]. The circle around the model indicates time of day, with 0 representing dawn. Components are positioned within the circle according to their approximate maximal transcript abundance in continuous light, with the exception of LKP2 and ZTL which are not transcribed in a circadian-dependent manner [105,108] and thus are represented by hexagons. Only interactions demonstrated experimentally are shown; positive interactions are shown with arrows, and negative interactions are indicated by perpendicular lines. Dotted lines indicate interactions assumed from a mathematical model but not conclusively demonstrated experimentally [72,73]. Components and interactions associated with light perception are shown in orange, and components and interactions involved in gating are shown in blue. The circadian regulator of ELF3 is unknown and therefore control of ELF3 by the clock is indicated by a dotted line.

Figure 5. Model to explain how multiple rhythms may be generated from similar oscillators

Gene 1 and Gene 2 are expressed in similar tissues, but have different free running periods and sensitivity to entrainment signals. (a) This could be due to multiple oscillators present within each cell. Each oscillator is based on the CCA1/LHY model shown in Figure 4, with multiple interlocking loops. Gene 1 expression is preferentially regulated by light which is mediated by an oscillator containing component A. Gene 2 expression is entrained primarily by temperature cycles, and is controlled via an oscillator containing component B. (b) Alternatively, different cells within the same tissue contain different oscillators. Circadian expression of Gene 1 and Gene 2 occur in different cells (X and Y), and the expression data obtained experimentally are an average of all cell types. Gene 1 expression is controlled by an oscillator with the cell-specific factor X, and Gene 2 expression is controlled by an oscillator containing cell-specific factor Y.