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In the cyanobacterium  Synechococcus elongatus  PCC 7942, circadian timing is transmitted from the KaiABC-based central oscillator to the transcription factor RpaA via the KaiC-interacting histidine kinase SasA to activate transcription, thereby generating rhythmic circadian gene expression. However, KaiC can also repress circadian gene expression, including its own. The mechanism and significance of this negative feedback regulation have been unclear. Here, we report a novel gene,  labA  (low-amplitude and bright), that is required for negative feedback regulation of KaiC. Disruption of  labA  abolished transcriptional repression caused by overexpression of KaiC and elevated the trough levels of circadian gene expression, resulting in a low-amplitude phenotype. In contrast, overexpression of  labA  significantly lowered circadian gene expression. Furthermore, genetic analysis indicated that  labA  and  sasA  function in parallel pathways to regulate  kaiBC  expression, whereas  rpaA  functions downstream from  labA  for  kaiBC  expression. These results suggest that temporal information from the KaiABC-based oscillator diverges into a LabA-dependent negative pathway and a SasA-dependent positive pathway, and then converges onto RpaA to generate robust circadian gene expression. It is likely that quantitative information of KaiC is transmitted to RpaA through LabA, whereas SasA mediates the state of the KaiABC-based oscillator.

labA: a novel gene required for negative feedback regulation of the cyanobacterial circadian clock protein KaiC