Arabidopsis circadian clock and photoperiodism: time to think about location

Abstract

Plants possess a circadian clock that enables them to coordinate internal biological events with external daily changes. Recent studies in Arabidopsis revealed that tissue-specific clock components exist and that the clock network architecture also varies within different organs. These findings indicate that the makeup of circadian clock(s) within a plant is quite variable. Plants utilize the circadian clock to measure day-length changes for regulating seasonal responses, such as flowering. To ensure that flowering occurs under optimum conditions, the clock regulates diurnal CONSTANS (CO) expression. Subsequently, CO protein induces FLOWERING LOCUS T (FT) expression which leads to flowering. It is emerging that both CO and FT expression are intricately controlled by groups of transcription factors with overlapping functions.

Figure 1

A model for the circadian clock and the photoperiodic flowering pathway in Arabidopsis. The most recently proposed clock architecture comprises three feedback loops (depicted in three different colors within the pale green circle that indicates the circadian clock). In the computational model CCA1 and LHY were treated as one functional unit, rather than two different proteins. Recent studies show that CCA1 and LHY form a functional unit by dimerization in vivo [62,63]. The CCA1/LHY-PRR7/9 loop is the only one that oscillates in mature roots under constant light condition [16••]. Several known clock components are not in the diagram due to their undetermined positions in the circuit. The diagram that is outside the pale green circle area denotes the clock-regulated photoperiodic pathway. Oval symbols depict proteins and overlapping ovals indicate protein complexes. Thick solid lines denote direct physical interactions, while thin solid lines denote genetic interactions. The dotted lines depict transcription and translation. The leaf cartoon indicates gene products that may be expressed mainly in leaf vascular tissues, based on studies of promoter-driven β-glucuronidase (GUS) reporter lines. The proteins that are directly involved in CO and FT gene expression and have gene and/or protein expression that is regulated by the circadian clock are shown with the clock cartoon symbol. The expression of genes which lack published gene or protein expression data under constant light conditions was analyzed using the publicly available microarray data at the DIURNAL project website [64]. Note that only a subset of the HAP genes shows daily oscillation in expression. All components in this diagram are likely expressed in the vasculature; therefore, this diagram may depict the connections between the circadian clock and photoperiodic flowering pathways in vascular tissues.

Figure 2

Schematic representation of the diurnal regulation of CO expression. In the morning, the expression levels of CDF1, CDF2, CDF3, and CDF5 genes are high. These CDF proteins likely bind to the CO promoter and are involved in suppression of CO transcription. The transcription of afternoon-phased GI and FKF1 is thought to be directly repressed by CCA1 and LHY. In the afternoon, the expression of these four CDF genes declines, and at least PRR5, PRR7 and PRR9 participate in the down-regulation of CDF1 expression. Decreasing levels of CCA1 and LHY release the repression FKF1 and GI and allow them to be expressed at high levels. Once FKF1 observes blue light, FKF1 forms a complex with GI. This complex is involved in the degradation of CDF1 and CDF2, and possibly other CDFs. Removal of CO repressors facilitates the expression of CO. At night, GI is degraded by a COP1 complex that contains ELF3. COP1 directly interacts with ELF3 to control ELF3 protein turnover [33•]. COP1 forms a complex with GI via ELF3 and also regulates GI stability. GI is required for the stabilization of FKF1 protein [29••], although it is not certain whether FKF1 is also degraded by COP1. Symbols have the same meaning as in Figure 1. Ub stands for ubiquitin.