Casein kinase 1 family regulates PRR5 and TOC1 in the Arabidopsis circadian clock
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 po...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS Jg. 116; H. 23; S. 11528 |
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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
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
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
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
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. |
|---|---|
| AbstractList | 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
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
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
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
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. 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.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. |
| Author | Yamaguchi, Junichiro Uehara, Takahiro N Mizutani, Yoshiyuki Mizoi, Junya Hirota, Tsuyoshi Yamaguchi-Shinozaki, Kazuko Nishiwaki-Ohkawa, Taeko Kay, Steve A Ito, Shogo Matsuo, Hiromi Suzuki, Takamasa Itami, Kenichiro Kuwata, Keiko Takao, Saori Saito, Ami N Yoshimura, Takashi Kinoshita, Toshinori Nakamichi, Norihito Sato, Ayato |
| Author_xml | – sequence: 1 givenname: Takahiro N surname: Uehara fullname: Uehara, Takahiro N organization: Department of Chemistry, Graduate School of Science, Nagoya University, 464-8602 Nagoya, Japan – sequence: 2 givenname: Yoshiyuki surname: Mizutani fullname: Mizutani, Yoshiyuki organization: Division of Biological Science, Graduate School of Science, Nagoya University, 464-8602 Nagoya, Japan – sequence: 3 givenname: Keiko surname: Kuwata fullname: Kuwata, Keiko organization: Institute of Transformative Bio-Molecules, Nagoya University, 464-8601 Nagoya, Japan – sequence: 4 givenname: Tsuyoshi surname: Hirota fullname: Hirota, Tsuyoshi organization: Japan Science and Technology Agency (JST) Precursory Research for Embryonic Science and Technology, 464-8602 Nagoya, Japan – sequence: 5 givenname: Ayato surname: Sato fullname: Sato, Ayato organization: Institute of Transformative Bio-Molecules, Nagoya University, 464-8601 Nagoya, Japan – sequence: 6 givenname: Junya surname: Mizoi fullname: Mizoi, Junya organization: Department of Applied Biological Chemistry, Graduate School of Life and Agricultural Sciences, The University of Tokyo, 113-8657 Tokyo, Japan – sequence: 7 givenname: Saori surname: Takao fullname: Takao, Saori organization: Institute of Transformative Bio-Molecules, Nagoya University, 464-8601 Nagoya, Japan – sequence: 8 givenname: Hiromi surname: Matsuo fullname: Matsuo, Hiromi organization: Institute of Transformative Bio-Molecules, Nagoya University, 464-8601 Nagoya, Japan – sequence: 9 givenname: Takamasa surname: Suzuki fullname: Suzuki, Takamasa organization: College of Bioscience and Biotechnology, Chubu University, 487-8501 Kasugai, Japan – sequence: 10 givenname: Shogo surname: Ito fullname: Ito, Shogo organization: Department of Botany, Graduate School of Science, Kyoto University, 606-8502 Kyoto, Japan – sequence: 11 givenname: Ami N surname: Saito fullname: Saito, Ami N organization: Department of Applied Chemistry, Waseda University, 169-8555 Tokyo, Japan – sequence: 12 givenname: Taeko surname: Nishiwaki-Ohkawa fullname: Nishiwaki-Ohkawa, Taeko organization: Graduate School of Bioagricultural Sciences, Nagoya University, 464-8601 Nagoya, Japan – sequence: 13 givenname: Kazuko surname: Yamaguchi-Shinozaki fullname: Yamaguchi-Shinozaki, Kazuko organization: Department of Applied Biological Chemistry, Graduate School of Life and Agricultural Sciences, The University of Tokyo, 113-8657 Tokyo, Japan – sequence: 14 givenname: Takashi orcidid: 0000-0001-7018-9652 surname: Yoshimura fullname: Yoshimura, Takashi organization: Graduate School of Bioagricultural Sciences, Nagoya University, 464-8601 Nagoya, Japan – sequence: 15 givenname: Steve A orcidid: 0000-0002-0402-2878 surname: Kay fullname: Kay, Steve A organization: Keck School of Medicine, University of Southern California, Los Angeles, CA 90033 – sequence: 16 givenname: Kenichiro surname: Itami fullname: Itami, Kenichiro organization: JST Exploratory Research for Advanced Technology, Itami Molecular Nanocarbon Project, Nagoya University, 464-8602 Nagoya, Japan – sequence: 17 givenname: Toshinori surname: Kinoshita fullname: Kinoshita, Toshinori organization: Institute of Transformative Bio-Molecules, Nagoya University, 464-8601 Nagoya, Japan – sequence: 18 givenname: Junichiro surname: Yamaguchi fullname: Yamaguchi, Junichiro email: junyamaguchi@waseda.jp, nnakamichi@itbm.nagoya-u.ac.jp organization: Department of Applied Chemistry, Waseda University, 169-8555 Tokyo, Japan; junyamaguchi@waseda.jp nnakamichi@itbm.nagoya-u.ac.jp – sequence: 19 givenname: Norihito surname: Nakamichi fullname: Nakamichi, Norihito email: junyamaguchi@waseda.jp, nnakamichi@itbm.nagoya-u.ac.jp organization: Institute of Transformative Bio-Molecules, Nagoya University, 464-8601 Nagoya, Japan |
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| Keywords | small molecule Arabidopsis circadian clock posttranslational regulation |
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| SubjectTerms | Arabidopsis - genetics Arabidopsis Proteins - genetics Casein Kinase I - genetics Circadian Clocks - genetics Circadian Rhythm - genetics Gene Expression Regulation, Plant - genetics Phosphorylation - genetics Protein Processing, Post-Translational - genetics Transcription Factors - genetics Transcription, Genetic - genetics |
| Title | Casein kinase 1 family regulates PRR5 and TOC1 in the Arabidopsis circadian clock |
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