Browse > Article
http://dx.doi.org/10.14348/molcells.2019.0199

GIGANTEA Regulates the Timing Stabilization of CONSTANS by Altering the Interaction between FKF1 and ZEITLUPE  

Hwang, Dae Yeon (Department of Life Sciences, Ajou University)
Park, Sangkyu (Department of Life Sciences, Ajou University)
Lee, Sungbeom (Advanced Radiation Technology Institute, Korea Atomic Energy Research Institute)
Lee, Seung Sik (Advanced Radiation Technology Institute, Korea Atomic Energy Research Institute)
Imaizumi, Takato (Department of Biology, University of Washington)
Song, Young Hun (Department of Life Sciences, Ajou University)
Abstract
Plants monitor changes in day length to coordinate their flowering time with appropriate seasons. In Arabidopsis, the diel and seasonal regulation of CONSTANS (CO) protein stability is crucial for the induction of FLOWERING LOCUS T (FT) gene in long days. FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 (FKF1) and ZEITLUPE (ZTL) proteins control the shape of CO expression profile antagonistically, although regulation mechanisms remain unknown. In this study, we show that GIGANTEA (GI) protein modulates the stability and nuclear function of FKF1, which is closely related to the stabilization of CO in the afternoon of long days. The abundance of FKF1 protein is decreased by the gi mutation, but increased by GI overexpression throughout the day. Unlike the previous report, the translocation of FKF1 to the nucleus was not prevented by ZTL overexpression. In addition, the FKF1-ZTL complex formation is higher in the nucleus than in the cytosol. GI interacts with ZTL in the nucleus, implicating the attenuation of ZTL activity by the GI binding and, in turn, the sequestration of FKF1 from ZTL in the nucleus. We also found that the CO-ZTL complex presents in the nucleus, and CO protein abundance is largely reduced in the afternoon by ZTL overexpression, indicating that ZTL promotes CO degradation by capturing FKF1 in the nucleus under these conditions. Collectively, our findings suggest that GI plays a pivotal role in CO stability for the precise control of flowering by coordinating balanced functional properties of FKF1 and ZTL.
Keywords
CONSTANS; FKF1; flowering; GIGANTEA; ZEITLUPE;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Alon, U. (2007). Network motifs: theory and experimental approaches. Nat. Rev. Genet. 8, 450-461.   DOI
2 Balasubramanian, S., Sureshkumar, S., Lempe, J., and Weigel, D. (2006). Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet. 2, e106.   DOI
3 Baudry, A., Ito, S., Song, Y.H., Strait, A.A., Kiba, T., Lu, S., Henriques, R., Pruneda-Paz, J.L., Chua, N.H., Tobin, E.M., et al. (2010). F-box proteins FKF1 and LKP2 act in concert with ZEITLUPE to control Arabidopsis clock progression. Plant Cell 22, 606-622.   DOI
4 Lee, C.M., Feke, A., Li, M.W., Adamchek, C., Webb, K., Pruneda-Paz, J., Bennett, E.J., Kay, S.A., and Gendron, J.M. (2018). Decoys untangle complicated redundancy and reveal targets of circadian clock F-Box proteins. Plant Physiol. 177, 1170-1186.   DOI
5 Mathieu, J., Warthmann, N., Kuttner, F., and Schmid, M. (2007). Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr. Biol. 17, 1055-1060.   DOI
6 Mishra, P. and Panigrahi, K.C. (2015). GIGANTEA: an emerging story. Front. Plant Sci. 6, 8.   DOI
7 Pudasaini, A., Shim, J.S., Song, Y.H., Shi, H., Kiba, T., Somers, D.E., Imaizumi, T., and Zoltowski, B.D. (2017). Kinetics of the LOV domain of ZEITLUPE determine its circadian function in Arabidopsis. Elife 6, e21646.   DOI
8 Corbesier, L., Vincent, C., Jang, S., Fornara, F., Fan, Q., Searle, I., Giakountis, A., Farrona, S., Gissot, L., Turnbull, C., et al. (2007). FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316, 1030-1033.   DOI
9 Fornara, F., Panigrahi, K.C., Gissot, L., Sauerbrunn, N., Ruhl, M., Jarillo, J.A., and Coupland, G. (2009). Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev. Cell 17, 75-86.   DOI
10 Nakagawa, T., Nakamura, S., Tanaka, K., Kawamukai, M., Suzuki, T., Nakamura, K., Kimura, T., and Ishiguro, S. (2008). Development of R4 gateway binary vectors (R4pGWB) enabling high-throughput promoter swapping for plant research. Biosci. Biotechnol. Biochem. 72, 624-629.   DOI
11 Samach, A., Onouchi, H., Gold, S.E., Ditta, G.S., Schwarz-Sommer, Z., Yanofsky, M.F., and Coupland, G. (2000). Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613-1616.   DOI
12 Sawa, M. and Kay, S.A. (2011). GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 108, 11698-11703.   DOI
13 Sawa, M., Nusinow, D.A., Kay, S.A., and Imaizumi, T. (2007). FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318, 261-265.   DOI
14 Song, Y.H., Estrada, D.A., Johnson, R.S., Kim, S.K., Lee, S.Y., MacCoss, M.J., and Imaizumi, T. (2014). Distinct roles of FKF1, GIGANTEA, and ZEITLUPE proteins in the regulation of Constans stability in Arabidopsis photoperiodic flowering. Proc. Natl. Acad. Sci. U. S. A. 111, 17672-17677.   DOI
15 Song, Y.H., Ito, S., and Imaizumi, T. (2013). Flowering time regulation: photoperiod- and temperature-sensing in leaves. Trends Plant Sci. 18, 575-583.   DOI
16 Song, Y.H., Kubota, A., Kwon, M.S., Covington, M.F., Lee, N., Taagen, E.R., Laboy Cintron, D., Hwang, D.Y., Akiyama, R., Hodge, S.K., et al. (2018). Molecular basis of flowering under natural long-day conditions in Arabidopsis. Nat. Plants 4, 824-835.   DOI
17 Hayama, R., Sarid-Krebs, L., Richter, R., Fernandez, V., Jang, S., and Coupland, G. (2017). PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein to promote flowering in response to day length. EMBO J. 36, 904-918.   DOI
18 Fukamatsu, Y., Mitsui, S., Yasuhara, M., Tokioka, Y., Ihara, N., Fujita, S., and Kiyosue, T. (2005). Identification of LOV KELCH PROTEIN2 (LKP2)-interacting factors that can recruit LKP2 to nuclear bodies. Plant Cell Physiol. 46, 1340-1349.   DOI
19 Goralogia, G.S., Liu, T.K., Zhao, L., Panipinto, P.M., Groover, E.D., Bains, Y.S., and Imaizumi, T. (2017). CYCLING DOF FACTOR 1 represses transcription through the TOPLESS co-repressor to control photoperiodic flowering in Arabidopsis. Plant J. 92, 244-262.   DOI
20 Han, L., Mason, M., Risseeuw, E.P., Crosby, W.L., and Somers, D.E. (2004). Formation of an SCF(ZTL) complex is required for proper regulation of circadian timing. Plant J. 40, 291-301.   DOI
21 Imaizumi, T., Schultz, T.F., Harmon, F.G., Ho, L.A., and Kay, S.A. (2005). FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309, 293-297.   DOI
22 Imaizumi, T., Tran, H.G., Swartz, T.E., Briggs, W.R., and Kay, S.A. (2003). FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426, 302-306.   DOI
23 Takase, T., Nishiyama, Y., Tanihigashi, H., Ogura, Y., Miyazaki, Y., Yamada, Y., and Kiyosue, T. (2011). LOV KELCH PROTEIN2 and ZEITLUPE repress Arabidopsis photoperiodic flowering under non-inductive conditions, dependent on FLAVIN-BINDING KELCH REPEAT F-BOX1. Plant J. 67, 608-621.   DOI
24 Song, Y.H., Shim, J.S., Kinmonth-Schultz, H.A., and Imaizumi, T. (2015). Photoperiodic flowering: time measurement mechanisms in leaves. Annu. Rev. Plant Biol. 66, 441-464.   DOI
25 Song, Y.H., Smith, R.W., To, B.J., Millar, A.J., and Imaizumi, T. (2012). FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science 336, 1045-1049.   DOI
26 Suarez-Lopez, P., Wheatley, K., Robson, F., Onouchi, H., Valverde, F., and Coupland, G. (2001). CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410, 1116-1120.   DOI
27 Tiwari, S.B., Shen, Y., Chang, H.C., Hou, Y., Harris, A., Ma, S.F., McPartland, M., Hymus, G.J., Adam, L., Marion, C., et al. (2010). The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol. 187, 57-66.   DOI
28 Valverde, F., Mouradov, A., Soppe, W., Ravenscroft, D., Samach, A., and Coupland, G. (2004). Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303, 1003-1006.   DOI
29 Jaeger, K.E. and Wigge, P.A. (2007). FT protein acts as a long-range signal in Arabidopsis. Curr. Biol. 17, 1050-1054.   DOI
30 Ito, S., Song, Y.H., and Imaizumi, T. (2012). LOV domain-containing F-Box proteins: light-dependent protein degradation modules in Arabidopsis. Mol. Plant 5, 47-56.
31 Kim, W.Y., Hicks, K.A., and Somers, D.E. (2005). Independent roles for EARLY FLOWERING 3 and ZEITLUPE in the control of circadian timing, hypocotyl length, and flowering time. Plant Physiol. 139, 1557-1569.   DOI
32 Jung, J.H., Seo, Y.H., Seo, P.J., Reyes, J.L., Yun, J., Chua, N.H., and Park, C.M. (2007). The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19, 2736-2748.   DOI
33 Kim, J., Geng, R., Gallenstein, R.A., and Somers, D.E. (2013). The F-box protein ZEITLUPE controls stability and nucleocytoplasmic partitioning of GIGANTEA. Development 140, 4060-4069.   DOI
34 Kim, W.Y., Fujiwara, S., Suh, S.S., Kim, J., Kim, Y., Han, L., David, K., Putterill, J., Nam, H.G., and Somers, D.E. (2007). ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449, 356-360.   DOI
35 Krahmer, J., Goralogia, G.S., Kubota, A., Zardilis, A., Johnson, R.S., Song, Y.H., MacCoss, M.J., Le Bihan, T., Halliday, K.J., Imaizumi, T., et al. (2019). Time-resolved interaction proteomics of the GIGANTEA protein under diurnal cycles in Arabidopsis. FEBS Lett. 593, 319-338.   DOI
36 Lee, B.D., Kim, M.R., Kang, M.Y., Cha, J.Y., Han, S.H., Nawkar, G.M., Sakuraba, Y., Lee, S.Y., Imaizumi, T., McClung, C.R., et al. (2017). The F-box protein FKF1 inhibits dimerization of COP1 in the control of photoperiodic flowering. Nat. Commun. 8, 2259.   DOI