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Originally published In Press as doi:10.1074/jbc.M803471200 on June 18, 2008

J. Biol. Chem., Vol. 283, Issue 34, 23073-23083, August 22, 2008
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Post-translational Regulation of the Arabidopsis Circadian Clock through Selective Proteolysis and Phosphorylation of Pseudo-response Regulator Proteins*Formula

Sumire Fujiwara{ddagger}12, Lei Wang{ddagger}1, Linqu Han{ddagger}3, Sung-Suk Suh{ddagger}, Patrice A. Salomé§4, C. Robertson McClung§, and David E. Somers{ddagger}5

From the {ddagger}Department of Plant Cellular and Molecular Biology/Plant Biotechnology Center, Ohio State University, Columbus, Ohio 43210 and the §Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755-3576

The circadian clock controls the period, phasing, and amplitude of processes that oscillate with a near 24-h rhythm. One core group of clock components in Arabidopsis that controls the pace of the central oscillator is comprised of five PRR (pseudo-response regulator) proteins whose biochemical function in the clock remains unclear. Peak expression of TOC1 (timing of cab expression 1)/PRR1, PRR3, PRR5, PRR7, and PRR9 are each phased differently over the course of the day and loss of any PRR protein alters period. Here we show that, together with TOC1, PRR5 is the only other likely proteolytic substrate of the E3 ubiquitin ligase SCFZTL within this PRR family. We further demonstrate a functional significance for the phosphorylated forms of PRR5, TOC1, and PRR3. Each PRR protein examined is nuclear-localized and is differentially phosphorylated over the circadian cycle. The more highly phosphorylated forms of PRR5 and TOC1 interact best with the F-box protein ZTL (ZEITLUPE), suggesting a mechanism to modulate their proteolysis. In vivo degradation of both PRR5 and ZTL is inhibited by blue light, likely the result of blue light photoperception by ZTL. TOC1 and PRR3 interact in vivo and phosphorylation of both is necessary for their optimal binding in vitro. Additionally, because PRR3 and ZTL both interact with TOC1 in vivo via the TOC1 N terminus, taken together these data suggest that the TOC1/PRR3 phosphorylation-dependent interaction may protect TOC1 from ZTL-mediated degradation, resulting in an enhanced amplitude of TOC1 cycling.


Received for publication, May 7, 2008 , and in revised form, June 12, 2008.

* This work was supported in part by National Science Foundation Grants MCB-0343887 (to C. R. M.) and IBN-0344377 and MCB-0544137 (to D. E. S.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Formula The on-line version of this article (available at http://www.jbc.org) contains supplemental Table S1 and Figs. S1 and S2.

1 Both authors contributed equally to this study.

2 Supported in part by Support for Long-term Visit from the Yamada Science Foundation.

3 Current address: Molecular, Cellular, and Developmental Biology, University of Michigan, 830 N. University, Ann Arbor, MI 48105.

4 Current address: Dept. of Molecular Biology, Max Planck Institute for Developmental Biology, Spemannstrasse 37-39, D-72076 Tübingen, Germany.

5 To whom correspondence should be addressed: 054 Rightmire Hall, 1060 Carmack Rd., Columbus, OH 43210. Fax: 614-292-5379; E-mail: somers.24{at}osu.edu.


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