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 inProceedings of the National Academy of Sciences - PNAS Vol. 116; no. 23; pp. 11528 - 11536
Main Authors 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
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 04.06.2019
SeriesPNAS Plus
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ISSN0027-8424
1091-6490
1091-6490
DOI10.1073/pnas.1903357116

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Summary: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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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)
ISSN:0027-8424
1091-6490
1091-6490
DOI:10.1073/pnas.1903357116