The KaiA protein of the cyanobacterial circadian oscillator is modulated by a redox-active cofactor

Wood, Thomas K.; Bridwell‐Rabb, Jennifer; Kim, Yong Ick; Gao, Tiyu; Chang, Yong Gang; LiWang, Andy; Barondeau, D.P.; Golden, Susan S.

doi:10.1073/pnas.0910141107

Cited by 77 publications

(79 citation statements)

References 34 publications

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“…Thus, natural variation in biosynthetic enzymes can feedback to alter circadian clock output, suggesting that the flow of information flow between the clock and metabolism is bidirectional. Similar links between clock function and metabolism have been previously reported (Rutter et al, 2002;Dodd et al, 2007;Duez and Staels, 2008;Kovac et al, 2009;Wood et al, 2010). Interestingly, we found that two completely separate genomics technologies, transcriptomics and metabolomics, that measure separate products, transcripts, and metabolites, independently identify the same genetic network within this Arabidopsis population.…”

Section: Plant Metabolism and Circadian Clock Outputssupporting

confidence: 56%

Network Quantitative Trait Loci Mapping of Circadian Clock Outputs Identifies Metabolic Pathway-to-Clock Linkages in Arabidopsis

et al. 2011

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Modern systems biology permits the study of complex networks, such as circadian clocks, and the use of complex methodologies, such as quantitative genetics. However, it is difficult to combine these approaches due to factorial expansion in experiments when networks are examined using complex methods. We developed a genomic quantitative genetic approach to overcome this problem, allowing us to examine the function(s) of the plant circadian clock in different populations derived from natural accessions. Using existing microarray data, we defined 24 circadian time phase groups (i.e., groups of genes with peak phases of expression at particular times of day). These groups were used to examine natural variation in circadian clock function using existing single time point microarray experiments from a recombinant inbred line population. We identified naturally variable loci that altered circadian clock outputs and linked these circadian quantitative trait loci to preexisting metabolomics quantitative trait loci, thereby identifying possible links between clock function and metabolism. Using single-gene isogenic lines, we found that circadian clock output was altered by natural variation in Arabidopsis thaliana secondary metabolism. Specifically, genetic manipulation of a secondary metabolic enzyme led to altered free-running rhythms. This represents a unique and valuable approach to the study of complex networks using quantitative genetics.

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Section: Plant Metabolism and Circadian Clock Outputssupporting

confidence: 56%

Network Quantitative Trait Loci Mapping of Circadian Clock Outputs Identifies Metabolic Pathway-to-Clock Linkages in Arabidopsis

et al. 2011

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“…Ectopic introduction of oxidized quinones can entrain the clock both in vivo and in vitro, and both KaiA and CikA play roles related to entrainment through binding of their PsR domains to oxidized quinones (71,72,(76)(77)(78). The aggregation state and/or stability of the proteins is affected by quinone binding in vivo (71,77). Still, the precise mechanism by which quinone binding influences the PTO is not currently well-understood.…”

Section: Metabolic Of Entrainment Of the Clockmentioning

confidence: 99%

“…As a result, the concentration of oxidized quinones rises rapidly but briefly when photosynthesis shuts down with the onset of darkness before other pathways restore the redox steady state (76). Ectopic introduction of oxidized quinones can entrain the clock both in vivo and in vitro, and both KaiA and CikA play roles related to entrainment through binding of their PsR domains to oxidized quinones (71,72,(76)(77)(78). The aggregation state and/or stability of the proteins is affected by quinone binding in vivo (71,77).…”

Section: Metabolic Of Entrainment Of the Clockmentioning

confidence: 99%

“…This metabolic entrainment of the cyanobacterial clock occurs in two ways: through sensitivity of the phosphorylation cycle to ATP/ADP ratios within the cell (75) and through the presence of nighttimeassociated photosynthetic metabolites (71,72,(76)(77)(78). The former entrainment cue occurs as a result of enzymatic sensitivity of the core oscillator to ATP/ADP ratios 72 , causing it to align with the maximal photosynthetic period at midday when this ratio is highest (75,79).…”

Section: Metabolic Of Entrainment Of the Clockmentioning

confidence: 99%

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Structure, function, and mechanism of the core circadian clock in cyanobacteria

Swan

Golden

LiWang

et al. 2018

Journal of Biological Chemistry

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“…The clock synchronizes to the environment through KaiA and a histidine protein kinase, CikA. Both proteins bind quinone cofactors, likely plastoquinone present in the photosynthetic membrane, that reflect the cellular redox state (12,13). KaiC activity also is modulated by the cellular ATP/ADP ratio (14), and both the cellular redox state and ATP/ADP ratio are dependent on the availability of external light.…”

mentioning

confidence: 99%

The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth

Diamond

Jun

Rubin

et al. 2015

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

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123

158

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Synechococcus elongatus PCC 7942 is a genetically tractable model cyanobacterium that has been engineered to produce industrially relevant biomolecules and is the best-studied model for a prokaryotic circadian clock. However, the organism is commonly grown in continuous light in the laboratory, and data on metabolic processes under diurnal conditions are lacking. Moreover, the influence of the circadian clock on diurnal metabolism has been investigated only briefly. Here, we demonstrate that the circadian oscillator influences rhythms of metabolism during diurnal growth, even though lightdark cycles can drive metabolic rhythms independently. Moreover, the phenotype associated with loss of the core oscillator protein, KaiC, is distinct from that caused by absence of the circadian output transcriptional regulator, RpaA (regulator of phycobilisome-associated A). Although RpaA activity is important for carbon degradation at night, KaiC is dispensable for those processes. Untargeted metabolomics analysis and glycogen kinetics suggest that functional KaiC is important for metabolite partitioning in the morning. Additionally, output from the oscillator functions to inhibit RpaA activity in the morning, and kaiC-null strains expressing a mutant KaiC phosphomimetic, KaiC-pST, in which the oscillator is locked in the most active output state, phenocopies a ΔrpaA strain. Inhibition of RpaA by the oscillator in the morning suppresses metabolic processes that normally are active at night, and kaiC-null strains show indications of oxidative pentose phosphate pathway activation as well as increased abundance of primary metabolites. Inhibitory clock output may serve to allow secondary metabolite biosynthesis in the morning, and some metabolites resulting from these processes may feed back to reinforce clock timing.C yanobacteria comprise a promising engineering platform for the production of fuels and industrial chemicals. These organisms already have been engineered to produce ethanol, isobutyraldehyde, alkanes, and hydrogen (1-4). However, the efficient industrial-scale application of these photosynthetic organisms will require their growth and maintenance in the outdoors where they will be subjected to light-dark (LD) cycles (5). Phototrophic cyanobacteria present a completely different engineering challenge relative to heterotrophic bacteria such as Escherichia coli: their cellular activities respond strongly to the presence and absence of light because their metabolism is centered on photosynthesis (6, 7). Diverse cyanobacteria also possess a true circadian clock that synchronizes with external LD cycles and has been demonstrated to drive both gene expression and metabolic rhythms (8-10). It is important to understand how signals from the external environment and the internal circadian clock are integrated to modulate metabolic processes in environmentally relevant LD cycles to optimize the engineering of these organisms. In this work we attempt to separate the influences of environment and circadian control using the cyan...

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The KaiA protein of the cyanobacterial circadian oscillator is modulated by a redox-active cofactor

Cited by 77 publications

References 34 publications

Network Quantitative Trait Loci Mapping of Circadian Clock Outputs Identifies Metabolic Pathway-to-Clock Linkages in Arabidopsis

Network Quantitative Trait Loci Mapping of Circadian Clock Outputs Identifies Metabolic Pathway-to-Clock Linkages in Arabidopsis

Structure, function, and mechanism of the core circadian clock in cyanobacteria

The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth

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