Response regulator homologues have complementary, light-dependent functions in the Arabidopsis circadian clock

Department of Biological Sciences, University of Warwick, Coventry, CV4 7AL, UK.
Planta (Impact Factor: 3.38). 12/2003; 218(1):159-62. DOI: 10.1007/s00425-003-1106-4
Source: PubMed

ABSTRACT TIMING OF CAB EXPRESSION 1 ( TOC1) functions with CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) in a transcriptional feedback loop that is important for the circadian clock in Arabidopsis thaliana (L.) Heynh. TOC1 and its four paralogues, the Arabidopsis PSEUDO-RESPONSE REGULATOR (PRR) genes, are expressed in an intriguing daily sequence. This was proposed to form a second feedback loop, similar to the interlocking clock gene circuits in other taxa. We show that prr9 and prr5 null mutants have reciprocal period defects for multiple circadian rhythms, consistent with subtly altered expression patterns of CCA1 and TOC1. The period defects are conditional on light quality and combine additively in double-mutant plants. Thus PRR9 and PRR5 modulate light input to the circadian clock but are neither uniquely required for rhythm generation nor form a linear series of mutual PRR gene regulation.

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    • "TOC1 protein is expressed in the evening and, in turn, activates CCA1 expression , partly by antagonizing a transcriptional repressor of CCA1, CCA1 HIKING EXPEDITION (CHE) of the TCP (for TEOSINTE BRANCHED1, CYCLOIDEA, and PCF) family (Pruneda-Paz et al., 2009). In addition to TOC1, numerous genetic studies have demonstrated the importance of other PRR genes in the circadian clock (Eriksson et al., 2003; Kaczorowski and Quail, 2003; Michael et al., 2003; Yamamoto et al., 2003; Farre et al., 2005; Nakamichi et al., 2005; Salome and McClung, 2005; Para et al., 2007; Ito et al., 2009). "
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    ABSTRACT: An interlocking transcriptional-translational feedback loop of clock-associated genes is thought to be the central oscillator of the circadian clock in plants. TIMING OF CAB EXPRESSION1 (also called PSEUDO-RESPONSE REGULATOR1 [PRR1]) and two MYB transcription factors, CIRCADIAN CLOCK ASSOCIATED1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), play pivotal roles in the loop. Genetic studies have suggested that PRR9, PRR7, and PRR5 also act within or close to the loop; however, their molecular functions remain unknown. Here, we demonstrate that PRR9, PRR7, and PRR5 act as transcriptional repressors of CCA1 and LHY. PRR9, PRR7, and PRR5 each suppress CCA1 and LHY promoter activities and confer transcriptional repressor activity to a heterologous DNA binding protein in a transient reporter assay. Using a glucocorticoid-induced PRR5-GR (glucorticoid receptor) construct, we found that PRR5 directly downregulates CCA1 and LHY expression. Furthermore, PRR9, PRR7, and PRR5 associate with the CCA1 and LHY promoters in vivo, coincident with the timing of decreased CCA1 and LHY expression. These results suggest that the repressor activities of PRR9, PRR7, and PRR5 on the CCA1 and LHY promoter regions constitute the molecular mechanism that accounts for the role of these proteins in the feedback loop of the circadian clock.
    The Plant Cell 03/2010; 22(3):594-605. DOI:10.1105/tpc.109.072892 · 9.58 Impact Factor
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    • "For instance, the expression levels of many clock genes (including CCA1, LHY, PRR7, PRR9, and GIGANTEA; GI) are upregulated by light (Wang and Tobin 1998; Martinez-Garcia et al. 2000; Eriksson et al. 2003; Farre et al. 2005; Locke et al. 2005; Farre and Kay 2007). Indeed, mutations in PRR7 and PRR9 only cause a long period in constantly lit conditions (Eriksson et al. 2003; Farre et al. 2005) suggesting that these genes act in pathways to modulate the effect of light on the entrainment of the circadian clock. Although little is known regarding the biochemical function of TOC1, recent years have seen steady gains in our knowledge of light-mediated protein stability of this protein. "
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    ABSTRACT: The rising and setting of the sun marks a transition between starkly contrasting environmental conditions for vegetative life. Given these differing diurnal and nocturnal environmental factors and the inherent regularity of the transition between the two, it is perhaps unsurprising that plants have developed an internal timing mechanism (known as a circadian clock) to allow modulation of gene expression and metabolism in response to external cues. Entrainment of the circadian clock, primarily via the detection of changes in light and temperature, maintains synchronization between the surrounding environment and the endogenous clock mechanism. In this review, recent advances in our understanding of the molecular workings of the plant circadian clock are discussed as are the input pathways necessary for entrainment of the clock machinery.
    Journal of Plant Biology 06/2009; 52(3):202-209. DOI:10.1007/s12374-009-9030-1 · 1.28 Impact Factor
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    • "PRR single mutants were found to cause a mild effect on period length, whereas some double and triple mutant combinations result in a severe clock phenotype: the double mutant prr9 prr7 displayed a longer period than either of the single mutants, and the prr5 prr7 double mutant phenotype was reported to exhibit very short to arrhythmic oscillations that became further compromised in the prr9 prr7 prr5 triple mutant (Farre et al., 2005; Fujimori et al., 2005; Nakamichi et al., 2005a, 2005b; Salome and McClung, 2005). Interestingly, combining the clock phenotype of the short-period prr5 mutation with the long-period prr9 mutation resulted in a wild-type period (Eriksson et al., 2003). Hence, despite their molecular similarity, not all PRRs are functionally equivalent, although some may have overlapping functions. "
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    ABSTRACT: The pseudoresponse regulators (PRRs) participate in the progression of the circadian clock in Arabidopsis thaliana. The founding member of the family, TIMING OF CAB EXPRESSION1 (TOC1), is an essential component of the transcriptional network that constitutes the core mechanism of the circadian oscillator. Recent data suggest a role in circadian regulation for all five members of the PRR family; however, the molecular function of TOC1 or any other PRRs remains unknown. In this work, we present evidence for the involvement of PRR3 in the regulation of TOC1 protein stability. PRR3 was temporally coexpressed with TOC1 under different photoperiods, yet its tissue expression was only partially overlapping with that of TOC1, as PRR3 appeared restricted to the vasculature. Decreased expression of PRR3 resulted in reduced levels of TOC1 protein, while overexpression of PRR3 caused an increase in the levels of TOC1, all without affecting the amount of TOC1 transcript. PRR3 was able to bind to TOC1 in yeast and in plants and to perturb TOC1 interaction with ZEITLUPE (ZTL), which targets TOC1 for proteasome-dependent degradation. Together, our results indicate that PRR3 might function to modulate TOC1 stability by hindering ZTL-dependent TOC1 degradation, suggesting the existence of local regulators of clock activity and adding to the growing importance of posttranslational regulation in the design of circadian timing mechanisms in plants.
    The Plant Cell 12/2007; 19(11):3462-73. DOI:10.1105/tpc.107.054775 · 9.58 Impact Factor
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