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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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 116; no. 23; pp. 11528 - 11536 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
04.06.2019
|
| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0027-8424 1091-6490 1091-6490 |
| DOI | 10.1073/pnas.1903357116 |
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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. |
|---|---|
| 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
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. 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. The mechanisms of eukaryotic circadian clocks rely on transcriptional-translational feedback loops (TTFLs), but components of TTFLs from different phylogenetic lineages are thought to be evolutionarily diverse. Posttranslational modification is also required for clock function, but those within the plant clock are less studied, likely due to genetic redundancy. Here, we identified a small synthetic molecule that lengthened the Arabidopsis circadian period. Using an affinity probe, we found that the molecule inhibited multiple members of the casein kinase I (CK1) family, which is also essential in animal, fungal, and algal clocks. The CK1 family modulated plant-specific clock-associated transcriptional repressors. With other studies, our results established the prominent role of CK1 family to control circadian clocks among vastly divergent phylogenetic lineages. 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 Kay, Steve A. Mizutani, Yoshiyuki Mizoi, Junya Hirota, Tsuyoshi Uehara, Takahiro N. Yamaguchi-Shinozaki, Kazuko Saito, Ami N. Nishiwaki-Ohkawa, Taeko Ito, Shogo Matsuo, Hiromi Suzuki, Takamasa Itami, Kenichiro Kuwata, Keiko Takao, Saori Yoshimura, Takashi Kinoshita, Toshinori Nakamichi, Norihito Sato, Ayato |
| Author_xml | – sequence: 1 givenname: Takahiro N. surname: Uehara fullname: Uehara, Takahiro N. – sequence: 2 givenname: Yoshiyuki surname: Mizutani fullname: Mizutani, Yoshiyuki – sequence: 3 givenname: Keiko surname: Kuwata fullname: Kuwata, Keiko – sequence: 4 givenname: Tsuyoshi surname: Hirota fullname: Hirota, Tsuyoshi – sequence: 5 givenname: Ayato surname: Sato fullname: Sato, Ayato – sequence: 6 givenname: Junya surname: Mizoi fullname: Mizoi, Junya – sequence: 7 givenname: Saori surname: Takao fullname: Takao, Saori – sequence: 8 givenname: Hiromi surname: Matsuo fullname: Matsuo, Hiromi – sequence: 9 givenname: Takamasa surname: Suzuki fullname: Suzuki, Takamasa – sequence: 10 givenname: Shogo surname: Ito fullname: Ito, Shogo – sequence: 11 givenname: Ami N. surname: Saito fullname: Saito, Ami N. – sequence: 12 givenname: Taeko surname: Nishiwaki-Ohkawa fullname: Nishiwaki-Ohkawa, Taeko – sequence: 13 givenname: Kazuko surname: Yamaguchi-Shinozaki fullname: Yamaguchi-Shinozaki, Kazuko – sequence: 14 givenname: Takashi surname: Yoshimura fullname: Yoshimura, Takashi – sequence: 15 givenname: Steve A. surname: Kay fullname: Kay, Steve A. – sequence: 16 givenname: Kenichiro surname: Itami fullname: Itami, Kenichiro – sequence: 17 givenname: Toshinori surname: Kinoshita fullname: Kinoshita, Toshinori – sequence: 18 givenname: Junichiro surname: Yamaguchi fullname: Yamaguchi, Junichiro – sequence: 19 givenname: Norihito surname: Nakamichi fullname: Nakamichi, Norihito |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31097584$$D View this record in MEDLINE/PubMed |
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| Keywords | small molecule Arabidopsis circadian clock posttranslational regulation |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Author contributions: J.Y. and N.N. designed research; T.N.U., Y.M., K.K., T.H., J.M., S.T., H.M., T.S., T.N.-O., J.Y., and N.N. performed research; T.N.U., Y.M., A.S., S.T., H.M., S.I., A.N.S., J.Y., and N.N. contributed new reagents/analytic tools; T.N.U., Y.M., K.K., T.H., J.M., S.T., H.M., T.S., T.N.-O., K.Y.-S., T.Y., S.A.K., K.I., T.K., J.Y., and N.N. analyzed data; and J.Y. and N.N. wrote the paper. 1T.N.U. and Y.M. contributed equally to this work. Edited by Susan S. Golden, University of California, San Diego, La Jolla, CA, and approved April 22, 2019 (received for review March 2, 2019) |
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| Snippet | The circadian clock provides organisms with the ability to adapt to daily and seasonal cycles. Eukaryotic clocks mostly rely on lineage-specific... The mechanisms of eukaryotic circadian clocks rely on transcriptional-translational feedback loops (TTFLs), but components of TTFLs from different phylogenetic... |
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| SubjectTerms | Arabidopsis Arabidopsis - genetics Arabidopsis Proteins - genetics Biological clocks Biological Sciences Casein Casein kinase I Casein Kinase I - genetics Circadian Clocks - genetics Circadian rhythm Circadian Rhythm - genetics Circadian rhythms Feedback loops Fungi Gene expression Gene Expression Regulation, Plant - genetics Genes Homology Kinases Organic chemistry Phosphorylation - genetics PNAS Plus Protein Processing, Post-Translational - genetics Proteins Proteomics Repressors Transcription factors Transcription Factors - genetics Transcription, Genetic - genetics |
| Title | Casein kinase 1 family regulates PRR5 and TOC1 in the Arabidopsis circadian clock |
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