A Cyanobacterial Circadian Timing Mechanism

Ditty, Jayna L.; Williams, Stanly B.; Golden, Susan S.

doi:10.1146/annurev.genet.37.110801.142716

Cited by 111 publications

(83 citation statements)

References 181 publications

(234 reference statements)

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“…Moreover, one would need to bring kaiBC expression under the control of a promoter that is constitutively active. However, most promoters of S. elongatus (37,43), and even many heterologous promoters from Escherichia coli (52), are influenced by the circadian clock. Nevertheless, a number of promoters have been reported that exhibit arrhythmic activity (43), and these might be possible candidates.…”

Section: Discussionmentioning

confidence: 99%

Robust circadian clocks from coupled protein-modification and transcription–translation cycles

Zwicker

Lubensky

Wolde

2010

Proc. Natl. Acad. Sci. U.S.A.

104

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The cyanobacterium Synechococcus elongatus uses both a protein phosphorylation cycle and a transcription-translation cycle to generate circadian rhythms that are highly robust against biochemical noise. We use stochastic simulations to analyze how these cycles interact to generate stable rhythms in growing, dividing cells. We find that a protein phosphorylation cycle by itself is robust when protein turnover is low. For high decay or dilution rates (and compensating synthesis rates), however, the phosphorylation-based oscillator loses its integrity. Circadian rhythms thus cannot be generated with a phosphorylation cycle alone when the growth rate, and consequently the rate of protein dilution, is high enough; in practice, a purely posttranslational clock ceases to function well when the cell doubling time drops below the 24-h clock period. At higher growth rates, a transcription-translation cycle becomes essential for generating robust circadian rhythms. Interestingly, although a transcription-translation cycle is necessary to sustain a phosphorylation cycle at high growth rates, a phosphorylation cycle can dramatically enhance the robustness of a transcriptiontranslation cycle at lower protein decay or dilution rates. In fact, the full oscillator built from these two tightly intertwined cycles far outperforms not just each of its two components individually, but also a hypothetical system in which the two parts are coupled as in textbook models of coupled phase oscillators. Our analysis thus predicts that both cycles are required to generate robust circadian rhythms over the full range of growth conditions.

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Section: Discussionmentioning

confidence: 99%

Robust circadian clocks from coupled protein-modification and transcription–translation cycles

Zwicker

Lubensky

Wolde

2010

Proc. Natl. Acad. Sci. U.S.A.

104

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“…A histidine protein kinase (HPK) called CikA (circadian input kinase) is a key component of the circadian clock input pathway in the cyanobacterium Synechococcus elongatus PCC 7942, which is the simplest organism, in terms of genome size and unicellular structure, known to possess a canonical circadian biological clock (Ditty et al ., 2003). The cikA gene was first identified from a Tn 5 transposon insertion mutant that showed a subtle defect in light-responsive regulation of photosynthesis genes; subsequently, the mutation was shown to have a more striking effect on circadian rhythms of gene expression (Schmitz et al ., 2000).…”

Section: Introductionmentioning

confidence: 99%

The pseudo‐receiver domain of CikA regulates the cyanobacterial circadian input pathway

Zhang

Dong

Golden

2006

Molecular Microbiology

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SummaryCikA (circadian input kinase) is a component of the cyanobacterial circadian clock that aids in synchronizing the endogenous oscillator with the external environment. cikA mutants of the prokaryotic circadian model organism Synechococcus elongatus PCC 7942 fail to reset the phase of the circadian rhythm of gene expression after an environmental time cue, and also exhibit reduced amplitude and shortened period of circadian oscillation. CikA has histidine protein kinase (HPK) activity that is modulated in vitro by GAF and pseudo -receiver (PsR) domains. Here we show that the PsR domain negatively regulates HPK activity in vivo and also serves as an interaction module to dock CikA at a specific subcellular location. Phenotypes conferred by alleles that encode CikA variants showed that all domains except the featureless Nterminus are required for CikA function. Overexpression of all alleles that encode the PsR domain, whether or not the HPK is functional, caused a dominant arrhythmic phenotype, whereas overexpressed variants that lack PsR did not. Subcellular localization of intact CikA identified a polar focus whereas a variant without PsR showed uniform distribution in the cell, consistent with a model in which PsR mediates interaction with other input pathway components.

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“…Systematic analysis of single promoters has yet to identify specific ciselements controlling expression phase (8,9), and neither random mutagenesis nor transposon insertion screens have identified trans-factors responsible for expression phase (10). Interestingly, several heterologous noncircadian promoters from Escherichia coli can drive circadian expression when integrated in S. elongatus, suggesting that a specific cis-sequence is not necessary for circadian promoter activity (11). The elusiveness of cis and trans factors has prompted the ''oscilloid model'' for circadian control of gene expression (12).…”

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confidence: 99%

Oscillations in supercoiling drive circadian gene expression in cyanobacteria

Vijayan

Zuzow

O’Shea

2009

Proc. Natl. Acad. Sci. U.S.A.

164

239

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The cyanobacterium Synechococcus elongatus PCC 7942 exhibits oscillations in mRNA transcript abundance with 24-h periodicity under continuous light conditions. The mechanism underlying these oscillations remains elusive-neither cis nor trans-factors controlling circadian gene expression phase have been identified. Here, we show that the topological status of the chromosome is highly correlated with circadian gene expression state. We also demonstrate that DNA sequence characteristics of genes that appear monotonically activated and monotonically repressed by chromosomal relaxation during the circadian cycle are similar to those of supercoiling-responsive genes in Escherichia coli. Furthermore, perturbation of superhelical status within the physiological range elicits global changes in gene expression similar to those that occur during the normal circadian cycle.circadian clock ͉ gene expression ͉ supercoiling ͉ cyanobacteria C ircadian rhythms in gene expression have been identified in many organisms. In general, 5-15% of an organism's transcriptome oscillates with 24-h periodicity in the absence of external cues such as light to dark or dark to light transitions (1). These transcriptional rhythms are controlled by an endogenous biological clock and allow organisms to schedule processes at appropriate times during the day and night cycle. The cyanobacterium Synechococcus elongatus PCC 7942 (hereafter, S. elongatus) is particularly striking because the majority of its gene expression is under circadian control in continuous light conditions. A ''promoter trap'' analysis using a bacterial luciferase reporter integrated at approximately 30,000 random loci showed circadian oscillations in bioluminescence at all 800 locations where bioluminescence signal was detected (2). A recent measurement of mRNA levels by microarray analysis demonstrated that at least 30% of transcript levels oscillated in circadian fashion (3). The discrepancy between promoter trap and microarray analysis is not surprising and is at least partially attributable to a combination of: (i) the limited time-resolution of microarrays and; (ii) the time-averaging of transcript levels observed in the bioluminescence output of promoter trap studies due to finite luciferase protein lifetime. The actual percentage of circadian transcripts in S. elongatus is likely between 30 and 100%; here we observe that 64% of transcripts oscillate with circadian periodicity (Fig. 1A).In S. elongatus, circadian oscillations in transcriptional activity require three genes, kaiA, kaiB, and kaiC, whose products comprise the core circadian oscillator. The proteins encoded by the kai genes interact with one another to generate circadian rhythms in KaiC phosphorylation at serine and threonine residues (4). Amazingly, an in vitro mixture of the Kai proteins and ATP reproduces in vivo oscillations in the phosphorylation state of KaiC (5). Inactivation of any kai gene abolishes circadian oscillations in both transcription and phosphorylation, and when kaiC is mutated such that p...

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A Cyanobacterial Circadian Timing Mechanism

Cited by 111 publications

References 181 publications

Robust circadian clocks from coupled protein-modification and transcription–translation cycles

Robust circadian clocks from coupled protein-modification and transcription–translation cycles

The pseudo‐receiver domain of CikA regulates the cyanobacterial circadian input pathway

Oscillations in supercoiling drive circadian gene expression in cyanobacteria

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