Circadian transcriptional regulation by the posttranslational oscillator without de novo clock gene expression in Synechococcus

Norimune Hosokawa, Tetsuhiro S. Hatakeyama, Takashi Kojima, Yoshiyuki Kikuchi, Hiroshi Ito, Hideo Iwasaki

    Research output: Contribution to journalArticle

    28 Citations (Scopus)

    Abstract

    Circadian rhythms are a fundamental property of most organisms, from cyanobacteria to humans. In the unicellular obligately photoautotrophic cyanobacterium Synechococcus elongatus PCC 7942, essentially all promoter activities are controlled by the KaiABC-based clock under continuous light conditions. When Synechococcus cells are transferred from the light to continuous dark (DD) conditions, the expression of most genes, including the clock genes kaiA and kaiBC, is rapidly down-regulated, whereas the KaiC phosphorylation cycle persists. Therefore, we speculated that the posttranslational oscillator might not drive the transcriptional circadian output without de novo expression of the kai genes. Here we show that the cyanobacterial clock regulates the transcriptional output even in the dark. The expression of a subset of genes in the genomes of cells grown in the dark was dramatically affected by kaiABC nullification, and the magnitude of dark induction was dependent on the time at which the cells were transferred from the light to the dark. Moreover, under DD conditions, the expression of some dark-induced gene transcripts exhibited temperature-compensated damped oscillations, which were nullified in kaiABC-null strains and were affected by a kaiC period mutation. These results indicate that the Kai protein-based posttranslational oscillator can drive the circadian transcriptional output even without the de novo expression of the clock genes.

    Original languageEnglish
    Pages (from-to)15396-15401
    Number of pages6
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume108
    Issue number37
    DOIs
    Publication statusPublished - 2011 Sep 13

    Fingerprint

    Synechococcus
    Cyanobacteria
    Gene Expression
    Light
    Genes
    Circadian Rhythm
    Phosphorylation
    Genome
    Mutation
    Temperature
    Proteins

    Keywords

    • Dark-induced genes
    • digA
    • hspA
    • kaiABC genes
    • pilH/rre7

    ASJC Scopus subject areas

    • General

    Cite this

    Circadian transcriptional regulation by the posttranslational oscillator without de novo clock gene expression in Synechococcus. / Hosokawa, Norimune; Hatakeyama, Tetsuhiro S.; Kojima, Takashi; Kikuchi, Yoshiyuki; Ito, Hiroshi; Iwasaki, Hideo.

    In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 108, No. 37, 13.09.2011, p. 15396-15401.

    Research output: Contribution to journalArticle

    Hosokawa, Norimune ; Hatakeyama, Tetsuhiro S. ; Kojima, Takashi ; Kikuchi, Yoshiyuki ; Ito, Hiroshi ; Iwasaki, Hideo. / Circadian transcriptional regulation by the posttranslational oscillator without de novo clock gene expression in Synechococcus. In: Proceedings of the National Academy of Sciences of the United States of America. 2011 ; Vol. 108, No. 37. pp. 15396-15401.
    @article{adf7f9b69fd44f7aacc5568cf39c9fcb,
    title = "Circadian transcriptional regulation by the posttranslational oscillator without de novo clock gene expression in Synechococcus",
    abstract = "Circadian rhythms are a fundamental property of most organisms, from cyanobacteria to humans. In the unicellular obligately photoautotrophic cyanobacterium Synechococcus elongatus PCC 7942, essentially all promoter activities are controlled by the KaiABC-based clock under continuous light conditions. When Synechococcus cells are transferred from the light to continuous dark (DD) conditions, the expression of most genes, including the clock genes kaiA and kaiBC, is rapidly down-regulated, whereas the KaiC phosphorylation cycle persists. Therefore, we speculated that the posttranslational oscillator might not drive the transcriptional circadian output without de novo expression of the kai genes. Here we show that the cyanobacterial clock regulates the transcriptional output even in the dark. The expression of a subset of genes in the genomes of cells grown in the dark was dramatically affected by kaiABC nullification, and the magnitude of dark induction was dependent on the time at which the cells were transferred from the light to the dark. Moreover, under DD conditions, the expression of some dark-induced gene transcripts exhibited temperature-compensated damped oscillations, which were nullified in kaiABC-null strains and were affected by a kaiC period mutation. These results indicate that the Kai protein-based posttranslational oscillator can drive the circadian transcriptional output even without the de novo expression of the clock genes.",
    keywords = "Dark-induced genes, digA, hspA, kaiABC genes, pilH/rre7",
    author = "Norimune Hosokawa and Hatakeyama, {Tetsuhiro S.} and Takashi Kojima and Yoshiyuki Kikuchi and Hiroshi Ito and Hideo Iwasaki",
    year = "2011",
    month = "9",
    day = "13",
    doi = "10.1073/pnas.1019612108",
    language = "English",
    volume = "108",
    pages = "15396--15401",
    journal = "Proceedings of the National Academy of Sciences of the United States of America",
    issn = "0027-8424",
    number = "37",

    }

    TY - JOUR

    T1 - Circadian transcriptional regulation by the posttranslational oscillator without de novo clock gene expression in Synechococcus

    AU - Hosokawa, Norimune

    AU - Hatakeyama, Tetsuhiro S.

    AU - Kojima, Takashi

    AU - Kikuchi, Yoshiyuki

    AU - Ito, Hiroshi

    AU - Iwasaki, Hideo

    PY - 2011/9/13

    Y1 - 2011/9/13

    N2 - Circadian rhythms are a fundamental property of most organisms, from cyanobacteria to humans. In the unicellular obligately photoautotrophic cyanobacterium Synechococcus elongatus PCC 7942, essentially all promoter activities are controlled by the KaiABC-based clock under continuous light conditions. When Synechococcus cells are transferred from the light to continuous dark (DD) conditions, the expression of most genes, including the clock genes kaiA and kaiBC, is rapidly down-regulated, whereas the KaiC phosphorylation cycle persists. Therefore, we speculated that the posttranslational oscillator might not drive the transcriptional circadian output without de novo expression of the kai genes. Here we show that the cyanobacterial clock regulates the transcriptional output even in the dark. The expression of a subset of genes in the genomes of cells grown in the dark was dramatically affected by kaiABC nullification, and the magnitude of dark induction was dependent on the time at which the cells were transferred from the light to the dark. Moreover, under DD conditions, the expression of some dark-induced gene transcripts exhibited temperature-compensated damped oscillations, which were nullified in kaiABC-null strains and were affected by a kaiC period mutation. These results indicate that the Kai protein-based posttranslational oscillator can drive the circadian transcriptional output even without the de novo expression of the clock genes.

    AB - Circadian rhythms are a fundamental property of most organisms, from cyanobacteria to humans. In the unicellular obligately photoautotrophic cyanobacterium Synechococcus elongatus PCC 7942, essentially all promoter activities are controlled by the KaiABC-based clock under continuous light conditions. When Synechococcus cells are transferred from the light to continuous dark (DD) conditions, the expression of most genes, including the clock genes kaiA and kaiBC, is rapidly down-regulated, whereas the KaiC phosphorylation cycle persists. Therefore, we speculated that the posttranslational oscillator might not drive the transcriptional circadian output without de novo expression of the kai genes. Here we show that the cyanobacterial clock regulates the transcriptional output even in the dark. The expression of a subset of genes in the genomes of cells grown in the dark was dramatically affected by kaiABC nullification, and the magnitude of dark induction was dependent on the time at which the cells were transferred from the light to the dark. Moreover, under DD conditions, the expression of some dark-induced gene transcripts exhibited temperature-compensated damped oscillations, which were nullified in kaiABC-null strains and were affected by a kaiC period mutation. These results indicate that the Kai protein-based posttranslational oscillator can drive the circadian transcriptional output even without the de novo expression of the clock genes.

    KW - Dark-induced genes

    KW - digA

    KW - hspA

    KW - kaiABC genes

    KW - pilH/rre7

    UR - http://www.scopus.com/inward/record.url?scp=80053082769&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=80053082769&partnerID=8YFLogxK

    U2 - 10.1073/pnas.1019612108

    DO - 10.1073/pnas.1019612108

    M3 - Article

    C2 - 21896749

    AN - SCOPUS:80053082769

    VL - 108

    SP - 15396

    EP - 15401

    JO - Proceedings of the National Academy of Sciences of the United States of America

    JF - Proceedings of the National Academy of Sciences of the United States of America

    SN - 0027-8424

    IS - 37

    ER -