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ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light

Nature volume 449, pages 356–360 (2007)Cite this article

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Abstract

The circadian clock is essential for coordinating the proper phasing of many important cellular processes. Robust cycling of key clock elements is required to maintain strong circadian oscillations of these clock-controlled outputs. Rhythmic expression of the Arabidopsis thaliana F-box protein ZEITLUPE (ZTL) is necessary to sustain a normal circadian period by controlling the proteasome-dependent degradation of a central clock protein, TIMING OF CAB EXPRESSION 1 (TOC1)1,2. ZTL messenger RNA is constitutively expressed, but ZTL protein levels oscillate with a threefold change in amplitude through an unknown mechanism3. Here we show that GIGANTEA (GI) is essential to establish and sustain oscillations of ZTL by a direct protein–protein interaction. GI, a large plant-specific protein with a previously undefined molecular role, stabilizes ZTL in vivo. Furthermore, the ZTL–GI interaction is strongly and specifically enhanced by blue light, through the amino-terminal flavin-binding LIGHT, OXYGEN OR VOLTAGE (LOV) domain of ZTL. Mutations within this domain greatly diminish ZTL–GI interactions, leading to strongly reduced ZTL levels. Notably, a C82A mutation in the LOV domain, implicated in the flavin-dependent photochemistry, eliminates blue-light-enhanced binding of GI to ZTL. These data establish ZTL as a blue-light photoreceptor, which facilitates its own stability through a blue-light-enhanced GI interaction. Because the regulation of GI transcription is clock-controlled, consequent GI protein cycling confers a post-translational rhythm on ZTL protein. This mechanism of establishing and sustaining robust oscillations of ZTL results in the high-amplitude TOC1 rhythms necessary for proper clock function.

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Figure 1: GIGANTEA positively regulates ZTL protein abundance.
Figure 2: Interactions of GI with ZTL require the LOV domain.
Figure 3: Blue-light-enhanced binding of GI and ZTL.
Figure 4: Post-transcriptional control of TOC1 protein by GI.

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Change history

  • 20 September 2007

    In the AOP version of this manuscript the LR and LB panels of ZTL in Fig. 3c were inadvertently inverted; this was corrected on 20 September 2007

References

  1. Somers, D. E., Schultz, T. F., Milnamow, M. & Kay, S. A. ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 101, 319–329 (2000)

    Article  CAS  Google Scholar 

  2. Mas, P., Kim, W. Y., Somers, D. E. & Kay, S. A. Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426, 567–570 (2003)

    Article  CAS  ADS  Google Scholar 

  3. Kim, W. Y., Geng, R. & Somers, D. E. Circadian phase-specific degradation of the F-box protein ZTL is mediated by the proteasome. Proc. Natl Acad. Sci. USA 100, 4933–4938 (2003)

    Article  CAS  ADS  Google Scholar 

  4. Fowler, S. et al. GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J. 18, 4679–4688 (1999)

    Article  CAS  Google Scholar 

  5. Park, D. et al. Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285, 1579–1582 (1999)

    Article  CAS  Google Scholar 

  6. Martin-Tryon, E. L., Kreps, J. A. & Harmer, S. L. GIGANTEA acts in blue light signaling and has biochemically separable roles in circadian clock and flowering time regulation. Plant Physiol. 143, 473–486 (2007)

    Article  CAS  Google Scholar 

  7. Gould, P. D. et al. The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell 18, 1177–1187 (2006)

    Article  CAS  Google Scholar 

  8. David, K. M., Armbruster, U., Tama, N. & Putterill, J. Arabidopsis GIGANTEA protein is post-transcriptionally regulated by light and dark. FEBS Lett. 580, 1193–1197 (2006)

    Article  CAS  Google Scholar 

  9. Nelson, D. C., Lasswell, J., Rogg, L. E., Cohen, M. A. & Bartel, B. FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101, 331–340 (2000)

    Article  CAS  Google Scholar 

  10. Schultz, T. F., Kiyosue, T., Yanovsky, M., Wada, M. & Kay, S. A. A role for LKP2 in the circadian clock of Arabidopsis. Plant Cell 13, 2659–2670 (2001)

    Article  CAS  Google Scholar 

  11. Zeng, L. R. et al. Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16, 2795–2808 (2004)

    Article  CAS  Google Scholar 

  12. Crosson, S. & Moffat, K. Structure of a flavin-binding plant photoreceptor domain: Insights into light-mediated signal transduction. Proc. Natl Acad. Sci. USA 98, 2995–3000 (2001)

    Article  CAS  ADS  Google Scholar 

  13. Froehlich, A. C., Liu, Y., Loros, J. J. & Dunlap, J. C. White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297, 815–819 (2002)

    Article  CAS  ADS  Google Scholar 

  14. He, Q. et al. White Collar-1, a DNA binding transcription factor and a light sensor. Science 297, 840–843 (2002)

    Article  CAS  ADS  Google Scholar 

  15. Imaizumi, T., Tran, H. G., Swartz, T. E., Briggs, W. R. & Kay, S. A. FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426, 302–306 (2003)

    Article  CAS  ADS  Google Scholar 

  16. Voinnet, O., Rivas, S., Mestre, P. & Baulcombe, D. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949–956 (2003)

    Article  CAS  Google Scholar 

  17. Kevei, E. et al. Forward genetic analysis of the circadian clock separates the multiple functions of ZEITLUPE. Plant Physiol. 140, 933–945 (2006)

    Article  CAS  Google Scholar 

  18. Han, L., Mason, M., Risseeuw, E. P., Crosby, W. L. & Somers, D. E. Formation of an SCF complex is required for proper regulation of circadian timing. Plant J. 40, 291–301 (2004)

    Article  CAS  Google Scholar 

  19. Somers, D. E., Kim, W. Y. & Geng, R. The F-box protein ZEITLUPE confers dosage-dependent control on the circadian clock, photomorphogenesis, and flowering time. Plant Cell 16, 769–782 (2004)

    Article  CAS  Google Scholar 

  20. Imaizumi, T., Schultz, T. F., Harmon, F. G., Ho, L. A. & Kay, S. A. FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309, 293–297 (2005)

    Article  CAS  ADS  Google Scholar 

  21. Salomon, M., Christie, J. M., Knieb, E., Lempert, U. & Briggs, W. R. Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. Biochemistry 39, 9401–9410 (2000)

    Article  CAS  Google Scholar 

  22. Strayer, C. et al. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289, 768–771 (2000)

    Article  CAS  ADS  Google Scholar 

  23. Harper, S. M., Neil, L. C. & Gardner, K. H. Structural basis of a phototropin light switch. Science 301, 1541–1544 (2003)

    Article  CAS  ADS  Google Scholar 

  24. Christie, J. M. et al. Arabidopsis NPH1: A flavoprotein with the properties of a photoreceptor for phototropism. Science 282, 1698–1701 (1998)

    Article  CAS  ADS  Google Scholar 

  25. Lee, C., Etchegaray, J. P., Cagampang, F. R., Loudon, A. S. & Reppert, S. M. Posttranslational mechanisms regulate the mammalian circadian clock. Cell 107, 855–867 (2001)

    Article  CAS  Google Scholar 

  26. Cardone, L. et al. Circadian clock control by SUMOylation of BMAL1. Science 309, 1390–1394 (2005)

    Article  CAS  ADS  Google Scholar 

  27. Mizoguchi, T. et al. Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17, 2255–2270 (2005)

    Article  CAS  Google Scholar 

  28. Cheng, X. F. & Wang, Z. Y. Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. Plant J. 43, 758–768 (2005)

    Article  CAS  Google Scholar 

  29. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998)

    Article  CAS  Google Scholar 

  30. Rubio, V. et al. An alternative tandem affinity purification strategy applied to Arabidopsis protein complex isolation. Plant J. 41, 767–778 (2005)

    Article  MathSciNet  CAS  Google Scholar 

  31. Seki, M. et al. Functional annotation of a full-length Arabidopsis cDNA collection. Science 296, 141–145 (2002)

    Article  ADS  Google Scholar 

  32. Seki, M., Carninci, P., Nishiyama, Y., Hayashizaki, Y. & Shinozaki, K. High-efficiency cloning of Arabidopsis full-length cDNA by biotinylated CAP trapper. Plant J. 15, 707–720 (1998)

    Article  CAS  Google Scholar 

  33. Ryu, J. S. et al. Phytochrome-specific type 5 phosphatase controls light signal flux by enhancing phytochrome stability and affinity for a signal transducer. Cell 120, 395–406 (2005)

    Article  CAS  Google Scholar 

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Acknowledgements

We thank S. L. Harmer for providing ztl-103 in advance of publication, S. Kay for TOC1-TOC1-YFP and LKP2-OX seed, D. Bisaro for the adenosine kinase antibody and J. Na for excellent technical assistance. T. Mizoguchi provided gi-3, gi-4, gi-5, gi-6, and GI-OX (Ler). W.-Y. K. was supported in part by a grant from the MOST/KOSEF to the Environmental Biotechnology National Core Research Center (BK21 program grant), Korea. S.F. was funded in part by Support for Long-term Visit from the Yamada Science Foundation. Support is acknowledged from a Korea Science and Engineering Foundation (KOSEF) grant funded by MOST and the National Core Research Center for Systems Biodynamics (to H.G.N.), from the NZ Marsden grant (to J.P.), and from the NSF (IBN and MCB) to D.E.S.

Author Contributions W.-Y.K., S.F., S.-S.S., L.H., J.K. and Y.K. performed experiments. W.-Y.K. and H.-G.N. co-directed and designed experiments. J.P., K.D. and H.G.N. contributed novel reagents. J.P., S.F. and H.G.N. commented on and edited the manuscript. D.E.S. directed research, designed experiments and wrote the manuscript.

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Author notes

  1. Woe-Yeon Kim and Sumire Fujiwara: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Plant Cellular and Molecular Biology/Plant Biotechnology Center, Ohio State University, 054 Rightmire Hall, 1060 Carmack Road, Columbus, Ohio 43210, USA,

    Woe-Yeon Kim, Sumire Fujiwara, Sung-Suk Suh, Linqu Han & David E. Somers

  2. Environmental Biotechnology National Core Research Center (BK21 program), Gyeongsang National University, Jinju 660-701, South Korea

    Woe-Yeon Kim

  3. Department of Life Science, Pohang University of Science and Technology, Pohang, Kyungbuk 790-784, South Korea,

    Jeongsik Kim, Yumi Kim & Hong Gil Nam

  4. School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand,

    Karine David & Joanna Putterill

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Correspondence to David E. Somers.

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Kim, WY., Fujiwara, S., Suh, SS. et al. ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449, 356–360 (2007). https://doi.org/10.1038/nature06132

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