Casein kinase 1 family regulates PRR5 and TOC1 in the Arabidopsis circadian clock

Takahiro N. Uehara, Yoshiyuki Mizutani, Keiko Kuwata, Tsuyoshi Hirota, Ayato Sato, Junya Mizoi, Saori Takao, Hiromi Matsuo, Takamasa Suzuki, Shogo Ito, Ami N. Saito, Taeko Nishiwaki-Ohkawa, Kazuko Yamaguchi-Shinozaki, Takashi Yoshimura, Steve A. Kay, Kenichiro Itami, Toshinori Kinoshita, Junichiro Yamaguchi, Norihito Nakamichi

研究成果: Article

抄録

The circadian clock provides organisms with the ability to adapt to daily and seasonal cycles. Eukaryotic clocks mostly rely on lineage-specific transcriptional-translational feedback loops (TTFLs). Posttranslational modifications are also crucial for clock functions in fungi and animals, but the posttranslational modifications that affect the plant clock are less understood. Here, using chemical biology strategies, we show that the Arabidopsis CASEIN KINASE 1 LIKE (CKL) family is involved in posttranslational modification in the plant clock. Chemical screening demonstrated that an animal CDC7/CDK9 inhibitor, PHA767491, lengthens the Arabidopsis circadian period. Affinity proteomics using a chemical probe revealed that PHA767491 binds to and inhibits multiple CKL proteins, rather than CDC7/CDK9 homologs. Simultaneous knockdown of Arabidopsis CKL-encoding genes lengthened the circadian period. CKL4 phosphorylated transcriptional repressors PSEUDO-RESPONSE REGULATOR 5 (PRR5) and TIMING OF CAB EXPRESSION 1 (TOC1) in the TTFL. PHA767491 treatment resulted in accumulation of PRR5 and TOC1, accompanied by decreasing expression of PRR5- and TOC1-target genes. A prr5 toc1 double mutant was hyposensitive to PHA767491-induced period lengthening. Together, our results reveal posttranslational modification of transcriptional repressors in plant clock TTFL by CK1 family proteins, which also modulate nonplant circadian clocks.

元の言語English
ページ(範囲)11528-11536
ページ数9
ジャーナルProceedings of the National Academy of Sciences of the United States of America
166
発行部数23
DOI
出版物ステータスPublished - 2019 1 1

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Casein Kinase I
Circadian Clocks
Post Translational Protein Processing
Arabidopsis
Proteomics
Genes
Proteins
Fungi
cellulose acetate-butyrate
PHA 767491

Keywords

    ASJC Scopus subject areas

    • General

    これを引用

    Casein kinase 1 family regulates PRR5 and TOC1 in the Arabidopsis circadian clock. / Uehara, Takahiro N.; Mizutani, Yoshiyuki; Kuwata, Keiko; Hirota, Tsuyoshi; Sato, Ayato; Mizoi, Junya; Takao, Saori; Matsuo, Hiromi; Suzuki, Takamasa; Ito, Shogo; Saito, Ami N.; Nishiwaki-Ohkawa, Taeko; Yamaguchi-Shinozaki, Kazuko; Yoshimura, Takashi; Kay, Steve A.; Itami, Kenichiro; Kinoshita, Toshinori; Yamaguchi, Junichiro; Nakamichi, Norihito.

    :: Proceedings of the National Academy of Sciences of the United States of America, 巻 166, 番号 23, 01.01.2019, p. 11528-11536.

    研究成果: Article

    Uehara, TN, Mizutani, Y, Kuwata, K, Hirota, T, Sato, A, Mizoi, J, Takao, S, Matsuo, H, Suzuki, T, Ito, S, Saito, AN, Nishiwaki-Ohkawa, T, Yamaguchi-Shinozaki, K, Yoshimura, T, Kay, SA, Itami, K, Kinoshita, T, Yamaguchi, J & Nakamichi, N 2019, 'Casein kinase 1 family regulates PRR5 and TOC1 in the Arabidopsis circadian clock' Proceedings of the National Academy of Sciences of the United States of America, 巻. 166, 番号 23, pp. 11528-11536. https://doi.org/10.1073/pnas.1903357116
    Uehara, Takahiro N. ; Mizutani, Yoshiyuki ; Kuwata, Keiko ; Hirota, Tsuyoshi ; Sato, Ayato ; Mizoi, Junya ; Takao, Saori ; Matsuo, Hiromi ; Suzuki, Takamasa ; Ito, Shogo ; Saito, Ami N. ; Nishiwaki-Ohkawa, Taeko ; Yamaguchi-Shinozaki, Kazuko ; Yoshimura, Takashi ; Kay, Steve A. ; Itami, Kenichiro ; Kinoshita, Toshinori ; Yamaguchi, Junichiro ; Nakamichi, Norihito. / Casein kinase 1 family regulates PRR5 and TOC1 in the Arabidopsis circadian clock. :: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; 巻 166, 番号 23. pp. 11528-11536.
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    abstract = "The circadian clock provides organisms with the ability to adapt to daily and seasonal cycles. Eukaryotic clocks mostly rely on lineage-specific transcriptional-translational feedback loops (TTFLs). Posttranslational modifications are also crucial for clock functions in fungi and animals, but the posttranslational modifications that affect the plant clock are less understood. Here, using chemical biology strategies, we show that the Arabidopsis CASEIN KINASE 1 LIKE (CKL) family is involved in posttranslational modification in the plant clock. Chemical screening demonstrated that an animal CDC7/CDK9 inhibitor, PHA767491, lengthens the Arabidopsis circadian period. Affinity proteomics using a chemical probe revealed that PHA767491 binds to and inhibits multiple CKL proteins, rather than CDC7/CDK9 homologs. Simultaneous knockdown of Arabidopsis CKL-encoding genes lengthened the circadian period. CKL4 phosphorylated transcriptional repressors PSEUDO-RESPONSE REGULATOR 5 (PRR5) and TIMING OF CAB EXPRESSION 1 (TOC1) in the TTFL. PHA767491 treatment resulted in accumulation of PRR5 and TOC1, accompanied by decreasing expression of PRR5- and TOC1-target genes. A prr5 toc1 double mutant was hyposensitive to PHA767491-induced period lengthening. Together, our results reveal posttranslational modification of transcriptional repressors in plant clock TTFL by CK1 family proteins, which also modulate nonplant circadian clocks.",
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    AU - Uehara, Takahiro N.

    AU - Mizutani, Yoshiyuki

    AU - Kuwata, Keiko

    AU - Hirota, Tsuyoshi

    AU - Sato, Ayato

    AU - Mizoi, Junya

    AU - Takao, Saori

    AU - Matsuo, Hiromi

    AU - Suzuki, Takamasa

    AU - Ito, Shogo

    AU - Saito, Ami N.

    AU - Nishiwaki-Ohkawa, Taeko

    AU - Yamaguchi-Shinozaki, Kazuko

    AU - Yoshimura, Takashi

    AU - Kay, Steve A.

    AU - Itami, Kenichiro

    AU - Kinoshita, Toshinori

    AU - Yamaguchi, Junichiro

    AU - Nakamichi, Norihito

    PY - 2019/1/1

    Y1 - 2019/1/1

    N2 - The circadian clock provides organisms with the ability to adapt to daily and seasonal cycles. Eukaryotic clocks mostly rely on lineage-specific transcriptional-translational feedback loops (TTFLs). Posttranslational modifications are also crucial for clock functions in fungi and animals, but the posttranslational modifications that affect the plant clock are less understood. Here, using chemical biology strategies, we show that the Arabidopsis CASEIN KINASE 1 LIKE (CKL) family is involved in posttranslational modification in the plant clock. Chemical screening demonstrated that an animal CDC7/CDK9 inhibitor, PHA767491, lengthens the Arabidopsis circadian period. Affinity proteomics using a chemical probe revealed that PHA767491 binds to and inhibits multiple CKL proteins, rather than CDC7/CDK9 homologs. Simultaneous knockdown of Arabidopsis CKL-encoding genes lengthened the circadian period. CKL4 phosphorylated transcriptional repressors PSEUDO-RESPONSE REGULATOR 5 (PRR5) and TIMING OF CAB EXPRESSION 1 (TOC1) in the TTFL. PHA767491 treatment resulted in accumulation of PRR5 and TOC1, accompanied by decreasing expression of PRR5- and TOC1-target genes. A prr5 toc1 double mutant was hyposensitive to PHA767491-induced period lengthening. Together, our results reveal posttranslational modification of transcriptional repressors in plant clock TTFL by CK1 family proteins, which also modulate nonplant circadian clocks.

    AB - The circadian clock provides organisms with the ability to adapt to daily and seasonal cycles. Eukaryotic clocks mostly rely on lineage-specific transcriptional-translational feedback loops (TTFLs). Posttranslational modifications are also crucial for clock functions in fungi and animals, but the posttranslational modifications that affect the plant clock are less understood. Here, using chemical biology strategies, we show that the Arabidopsis CASEIN KINASE 1 LIKE (CKL) family is involved in posttranslational modification in the plant clock. Chemical screening demonstrated that an animal CDC7/CDK9 inhibitor, PHA767491, lengthens the Arabidopsis circadian period. Affinity proteomics using a chemical probe revealed that PHA767491 binds to and inhibits multiple CKL proteins, rather than CDC7/CDK9 homologs. Simultaneous knockdown of Arabidopsis CKL-encoding genes lengthened the circadian period. CKL4 phosphorylated transcriptional repressors PSEUDO-RESPONSE REGULATOR 5 (PRR5) and TIMING OF CAB EXPRESSION 1 (TOC1) in the TTFL. PHA767491 treatment resulted in accumulation of PRR5 and TOC1, accompanied by decreasing expression of PRR5- and TOC1-target genes. A prr5 toc1 double mutant was hyposensitive to PHA767491-induced period lengthening. Together, our results reveal posttranslational modification of transcriptional repressors in plant clock TTFL by CK1 family proteins, which also modulate nonplant circadian clocks.

    KW - Arabidopsis

    KW - Circadian clock

    KW - Posttranslational regulation

    KW - Small molecule

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