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Structure of the SHR–SCR heterodimer bound to the BIRD/IDD transcriptional factor JKD

Nature Plants volume 3, Article number: 17010 (2017) Cite this article

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Abstract

The plant-specific GAI, RGA and SCR (GRAS) family proteins play critical roles in plant development and signalling. Two GRAS proteins, SHORT-ROOT (SHR) and SCARECROW (SCR), cooperatively direct asymmetric cell division and the patterning of root cell types by transcriptional control in conjunction with BIRD/INDETERMINATE DOMAIN (IDD) transcription factors, although precise details of these specific interactions and actions remain unknown. Here, we present the crystal structures of the SHR–SCR binary and JACKDAW (JKD)/IDD10–SHR–SCR ternary complexes. Each GRAS domain comprises one α/β core subdomain with an α-helical cap that mediates heterodimerization by forming an intermolecular helix bundle. The α/β core subdomain of SHR forms the BIRD binding groove, which specifically recognizes the zinc fingers of JKD. We identified a conserved SHR-binding motif in 13 BIRD/IDD transcription factors. Our results establish a structural basis for GRAS–GRAS and GRAS–BIRD interactions and provide valuable clues towards our understanding of these regulators, which are involved in plant-specific signalling networks.

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Figure 1: Structure of the heterodimeric SHR–SCR complex.
Figure 2: Structural comparison and GRAS conserved motifs.
Figure 3: The SHR and SCR interaction.
Figure 4: Zinc fingers of MGP and JKD essential for SHR–SCR binding and DNA binding.
Figure 5: BIRD/IDD ZFs bind SHR of the SHR–SCR complex.
Figure 6: A DNA-bound model of the ZFs of BIRD/IDD transcription factors bound to the SHR–SCR complex.

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Acknowledgements

We thank R. Kurata for technical support in performing the MALDI-TOF MS analysis. We appreciate access to BL41XU and BL44XU beamlines at the SPring-8 synchrotron facility for the provision of synchrotron data collection facilities (proposal nos. 2013A6844, 2013B1288, 2013B6844, 2014A 1283 and 2014A6944). The cDNAs were provided by RIKEN BRC through the National Bio-Resource Project of the MEXT, Japan. This work was supported by a Grant-in-Aid for Scientific Research on Innovative Areas ‘Structural Cell Biology’ (to T.H.), a Grant-in-Aid for Scientific Research (C) (to Y.H.) from MEXT, Japan, the Core Research for Evolutionary Science and Technology (CREST), the Japan Science and Technology Agency (to Y.H.) and the National Institutes of Health, United States (R01 GM100051 to T.-p.S.).

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  1. Seiji Takayama

    Present address: †Present address: Department of Applied Biological Chemistry, the University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan.,

Authors and Affiliations

  1. Structural Biology Laboratory, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, 630-0192, Nara, Japan

    Yoshinori Hirano, Masahiro Nakagawa, Tomoe Suyama, Kohji Murase, Maya Shirakawa & Toshio Hakoshima

  2. The Laboratory of Intercellular Communication, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, 630-0192, Nara, Japan

    Kohji Murase & Seiji Takayama

  3. Department of Biology, Duke University, Durham, 27708, North Carolina, USA

    Tai-ping Sun

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Contributions

Y.H. and T.H. conceived and designed the project. Y.H. was responsible for construct design for the protein preparations. M.S., Y.H. and M.N. prepared the DNA constructs. Y.H., M.N. and T.S. performed protein biochemistry, crystallization and X-ray data collection. Y.H. solved and refined the structures. K.M. performed in vivo binding assay supervised by S.T., Y.H., M.N., T.S. and T.H. interpreted data. Y.H., T.-p.S. and T.H. wrote the manuscript.

Corresponding author

Correspondence to Toshio Hakoshima.

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Supplementary Information 1–3, Supplementary Table 1, Supplementary Figures 1–12, Supplementary Figure Legends 1–12. (PDF 4184 kb)

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Hirano, Y., Nakagawa, M., Suyama, T. et al. Structure of the SHR–SCR heterodimer bound to the BIRD/IDD transcriptional factor JKD. Nature Plants 3, 17010 (2017). https://doi.org/10.1038/nplants.2017.10

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