An expanding universe of circadian networks in higher plants

Abstract

Extensive circadian clock networks regulate almost every biological process in plants. Clock-controlled physiological responses are coupled with daily oscillations in environmental conditions resulting in enhanced fitness and growth vigor. Identification of core clock components and their associated molecular interactions has established the basic network architecture of plant clocks, which consists of multiple interlocked feedback loops. A hierarchical structure of transcriptional feedback overlaid with regulated protein turnover sets the pace of the clock and ultimately drives all clock-controlled processes. Although originally described as linear entities, increasing evidence suggests that many signaling pathways can act as both inputs and outputs within the overall network. Future studies will determine the molecular mechanisms involved in these complex regulatory loops.

Figure 1

Model of the circadian clock in Arabidopsis. Transcriptional and post-translational mechanisms define the basic architecture of Arabidopsis clock. The core feedback loop consists of two Myb-transcription factors, CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), which negatively regulate the expression of TIMING OF CAB EXPRESSION 1 (TOC1). TOC1 been proposed to activate the expression of CCA1 and LHY. An additional module within this loop includes the reciprocal repression between CCA1 and CCA1 HIKING EXPEDITION (CHE). TOC1 likely antagonizes CHE through a direct protein interaction. Two additional phase-specific feedback loops have been proposed. In the morning loop CCA1 and LHY activate the expression of PSEUDORESPONSE REGULATORS 7 and 9 (PRR7 and PRR9), which in turn repress CCA1 and LHY. In the evening loop TOC1 represses an unknown component generically named Y (GIGANTEA (GI) appear to be part of Y), which in turn activates the expression of TOC1. TOC1 levels are controlled by proteasomal degradation mediated by the F-box protein ZEITLUPE (ZTL). This mechanism is modulated by GI and the competitive interaction between ZTL and PSEUDORESPONSE REGULATOR 3 (PRR3) with TOC1. The interaction between TOC1 and PRR3 is likely favored by the phosphorylation of these proteins. For clarity, clock components that cannot be placed with confidence to these feedback loops were omitted. Further details on the regulatory mechanisms shown here can be found throughout the text.

Figure 2

Emerging model of the plant circadian system. Although initially outlined as three modules (clock-input pathways, circadian oscillator, and clock-output pathways) organized in a unidirectional path, accumulated experimental evidence indicates that the circadian system constitutes an expansive regulatory network where the circadian oscillator and major plant signaling modules (red circles) are regulated in a reciprocal fashion (black curved arrows, thicker lines denote the higher importance of these pathways as clock inputs). Main input signals such as light and temperature are also subject to clock regulation and many clock-output pathways often feedback to modulate the function of the circadian oscillator. This mechanism and the multiple interconnections between signaling modules (red dotted arrows) provide an integrated system to sense environmental cues (black dashed frame and arrows) and control plant physiology accordingly.