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14-3-3 proteins act as intracellular receptors for rice Hd3a florigen

Nature volume 476, pages 332–335 (2011)Cite this article

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Abstract

‘Florigen’ was proposed 75 years ago1 to be synthesized in the leaf and transported to the shoot apex, where it induces flowering. Only recently have genetic and biochemical studies established that florigen is encoded by FLOWERING LOCUS T (FT), a gene that is universally conserved in higher plants2,3,4. Nonetheless, the exact function of florigen during floral induction remains poorly understood and receptors for florigen have not been identified. Here we show that the rice FT homologue Hd3a5 interacts with 14-3-3 proteins in the apical cells of shoots, yielding a complex that translocates to the nucleus and binds to the Oryza sativa (Os)FD1 transcription factor, a rice homologue of Arabidopsis thaliana FD. The resultant ternary ‘florigen activation complex’ (FAC) induces transcription of OsMADS15, a homologue of A. thaliana APETALA1 (AP1), which leads to flowering. We have determined the 2.4 Å crystal structure of rice FAC, which provides a mechanistic basis for florigen function in flowering. Our results indicate that 14-3-3 proteins act as intracellular receptors for florigen in shoot apical cells, and offer new approaches to manipulate flowering in various crops and trees.

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Figure 1: Interactions among Hd3a, GF14 and OsFD1.
Figure 2: Structure of the florigen activation complex.
Figure 3: The Hd3a–GF14b complex enters the nucleus to interact with OsFD1.
Figure 4: 14-3-3 interaction is required for OsMADS15 activation by Hd3a and OsFD1.

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Biological Magnetic Resonance Data Bank

Protein Data Bank

Data deposits

The atomic coordinates, structure factors and NMR data have been deposited in the Protein Data Bank (accession number 3AXY) and Biological Magnetic Resonance Bank (accession number 11442).

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  • 08 August 2011

    The Supplementary Figures and Tables were missing from the original file posted online and were added on 8 August 2011.

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Acknowledgements

We thank Y. Takahashi for the anti-14-3-3 antibody and S. Takayama for the BiFC vectors. We are grateful to I. Smith for critical reading of the manuscript. We also thank N. Inada for FRET measurement; Y. Nishio, Y. Ohno, E. Kawano and M. Kanda for technical assistance; Y. Tamaki, Y. Konomi and J. Naritomi for rice transformation; M. Yoneyama, H. Kinoshita and A. Yasuba for sample preparation; J. Tsukamoto for mass spectroscopy analysis; H. Fukada for ITC measurement; K. Takeshita and Y. Hara for crystallization; and members of the Laboratory of Plant Molecular Genetics and the Laboratory of Biophysics at Nara Institute of Science and Technology (NAIST) for discussions. We thank beamline staff of BL41XU and BL44XU at SPring-8 and Photon Factory for data collection. We also thank Academia Sinica and National Synchrotron Radiation Research Center (Taiwan) for use of the MX225-HE detector at BL44XU. This work was supported in part by grants from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) through the Target Proteins Research Program, by the Global COE Program at NAIST, by Grants-in-Aid for Scientific Research to I.O., C.K. and K.S., by Grants-in-Aid for Scientific Research on Priority Areas to K.S. and by the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry from Bio-oriented Research Advancement Institution (BRAIN) to H.T.

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Author notes

  1. Yekti Asih Purwestri

    Present address: Present address: Faculty of Biology, Universitas Gadjah Mada, Yogyakarta 55281, Indonesia.,

  2. Ken-ichiro Taoka, Izuru Ohki and Hiroyuki Tsuji: These authors contributed equally to this work.

Authors and Affiliations

  1. Laboratory of Plant Molecular Genetics, Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0192, Japan

    Ken-ichiro Taoka, Hiroyuki Tsuji, Tomoko Yanase, Midori Yamaguchi, Chika Nakashima, Yekti Asih Purwestri, Shojiro Tamaki, Yuka Ogaki, Chihiro Shimada & Ko Shimamoto

  2. Laboratory of Biophysics, Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0192, Japan

    Izuru Ohki, Kyoko Furuita, Kokoro Hayashi & Chojiro Kojima

  3. Institute for Protein Research, Osaka University, 3-2 Yamadaoka, Suita, Osaka 565-0871, Japan

    Atsushi Nakagawa & Chojiro Kojima

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Contributions

K.T., I.O., H.T., K.F., K.H., T.Y., M.Y., C.N., Y.A.P., S.T., Y.O. and C.S. performed experiments; I.O. conceived the idea that 14-3-3 mediates the interaction between Hd3a and OsFD1; K.T., I.O., H.T., A.N., C.K. and K.S. analysed data; and K.T., I.O., H.T., C.K. and K.S. wrote the paper. C.K. and K.S. contributed equally to this work.

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Correspondence to Chojiro Kojima or Ko Shimamoto.

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Supplementary information

Supplementary Information

This file contains Supplementary Text 1 to 7, additional references, Supplementary Figures 1 to 30 with legends and Supplementary Tables 1 to 6. The Supplementary Figures and Tables were missing from the original file posted online and were added on 8 August 2011. (PDF 20553 kb)

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Taoka, Ki., Ohki, I., Tsuji, H. et al. 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476, 332–335 (2011). https://doi.org/10.1038/nature10272

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