Mapping the Core of the Arabidopsis Circadian Clock Defines the Network Structure of the Oscillator

Abstract

In many organisms, the circadian clock is composed of functionally coupled morning and evening oscillators. In Arabidopsis, oscillator coupling relies on a core loop in which the evening oscillator component TIMING OF CAB EXPRESSION 1 (TOC1) was proposed to activate a subset of morning-expressed oscillator genes. Here, we show that TOC1 does not function as an activator but rather as a general repressor of oscillator gene expression. Repression occurs through TOC1 rhythmic association to the promoters of the oscillator genes. Hormone-dependent induction of TOC1 and analysis of RNA interference plants show that TOC1 prevents the activation of morning-expressed genes at night. Our study overturns the prevailing model of the Arabidopsis circadian clock, showing that the morning and evening oscillator loops are connected through the repressing activity of TOC1.

PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein to promote flowering in response to day length

“…The abundance of their transcripts and proteins exhibit circadian rhythms, and under diurnal conditions, they peak in expression sequentially at 2–3 h intervals during the light period in the order PRR9 , PRR7 , PRR5 , PRR3 , and TOC1 (Matsushika et al , 2000; Fujiwara et al , 2008). PRR9, PRR7, PRR5, and TOC1 proteins are degraded during the night, so they mainly accumulate during the day when they repress transcription of genes encoding other clock components such as LATE ELONGATED HYPOCOTYL (LHY) and CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) (Mas et al , 2003b; Farré & Kay, 2007; Ito et al , 2007; Kiba et al , 2007; Nakamichi et al , 2010; Huang et al , 2012). Mutations in the PRR genes also delay flowering under LDs (Nakamichi et al , 2005; Ito et al , 2008), but double or triple mutants exhibit much stronger phenotypes suggesting functional redundancy between the genes (Nakamichi et al , 2005, p. 549; Ito et al , 2008).…”

SND1 Transcription Factor-Directed Quantitative Functional Hierarchical Genetic Regulatory Network in Wood Formation in Populus trichocarpa

“…While TFs typically act cooperatively and combinatorially on their cis-regulatory DNA targets for gene expression (Müller, 2001; Levine and Tjian, 2003;Chen and Rajewsky, 2007;Hobert, 2008), a single TF may also target hundreds of genes (Chen and Rajewsky, 2007;Kaufmann et al, 2009;Demura and Ye, 2010;Huang et al, 2012;Li et al, 2012). Many TFs also target their own genes (autoactivation or repression) (Becskei and Serrano, 2000;Wray et al, 2003;Li et al, 2012).…”

“…The regulatory effects of some of these interactions were demonstrated through perturbation or induction of the specific TF in transgenics or mutants (Pruneda-Paz et al, 2009;Zheng et al, 2009;Bassel et al, 2012;Huang et al, 2012;Kumar et al, 2012). Knowledge of the TF-DNA interactions in species other than Arabidopsis is limited.…”

A Constitutively Active Allele of Phytochrome B Maintains Circadian Robustness in the Absence of Light

“…PRR9, whose transcription is itself light induced (Ito et al, 2003;Jones et al, 2012), represses expression of CCA1 and LHY in partnership with the later-phased PRR7, PRR5, and TIMING OF CAB1 (TOC1; Matsushika et al, 2000;Nakamichi et al, 2010). Later in the subjective day, TOC1 and REVEILLE8 act as negative and positive transcription factors, respectively, that act to reinforce the robust oscillations of circadian genes (Farinas and Más, 2011;Gendron et al, 2012;Huang et al, 2012;Hsu et al, 2013). In addition to acute photoreceptor-mediated effects on the clock, it is well established that increasing fluence rates of light under constant conditions quickens circadian pace in plants, as well as many other species (Aschoff, 1960).…”