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

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.

[1]  N. Pavletich,et al.  Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A , 1991, Science.

[2]  P. Benfey,et al.  Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. , 1993, Development.

[3]  P. Benfey,et al.  Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis , 1995 .

[4]  P. Benfey,et al.  The SCARECROW Gene Regulates an Asymmetric Cell Division That Is Essential for Generating the Radial Organization of the Arabidopsis Root , 1996, Cell.

[5]  Z. Otwinowski,et al.  Processing of X-ray diffraction data collected in oscillation mode. , 1997, Methods in enzymology.

[6]  S. Doublié.  Preparation of selenomethionyl proteins for phase determination. , 1997, Methods in enzymology.

[7]  P. Benfey,et al.  The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. , 1999, The Plant journal : for cell and molecular biology.

[8]  Liisa Holm,et al.  DaliLite workbench for protein structure comparison , 2000, Bioinform..

[9]  Philip N Benfey,et al.  The SHORT-ROOT Gene Controls Radial Patterning of the Arabidopsis Root through Radial Signaling , 2000, Cell.

[10]  C. Pabo,et al.  Design and selection of novel Cys2His2 zinc finger proteins. , 2001, Annual review of biochemistry.

[11]  P. Benfey,et al.  Intercellular movement of the putative transcription factor SHR in root patterning , 2001, Nature.

[12]  Jennifer L. Martin,et al.  SAM (dependent) I AM: the S-adenosylmethionine-dependent methyltransferase fold. , 2002, Current opinion in structural biology.

[13]  Takeharu Nagai,et al.  Shift anticipated in DNA microarray market , 2002, Nature Biotechnology.

[14]  George M Sheldrick,et al.  Substructure solution with SHELXD. , 2002, Acta crystallographica. Section D, Biological crystallography.

[15]  S. Sabatini,et al.  SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. , 2003, Genes & development.

[16]  B. Scheres,et al.  Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. , 2004, Genes & development.

[17]  C. Joshi,et al.  Conserved sequence motifs in plant S-adenosyl-L-methionine-dependent methyltransferases , 1998, Plant Molecular Biology.

[18]  Kevin Cowtan,et al.  research papers Acta Crystallographica Section D Biological , 2005 .

[19]  Cordelia Bolle,et al.  The role of GRAS proteins in plant signal transduction and development , 2004, Planta.

[20]  S. Hake,et al.  The maize ID1 flowering time regulator is a zinc finger protein with novel DNA binding properties. , 2004, Nucleic acids research.

[21]  P. Benfey,et al.  Whole-Genome Analysis of the SHORT-ROOT Developmental Pathway in Arabidopsis , 2006, PLoS biology.

[22]  Viktoriya Coneva,et al.  The maize INDETERMINATE1 flowering time regulator defines a highly conserved zinc finger protein family in higher plants , 2006, BMC Genomics.

[23]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

[24]  Teva Vernoux,et al.  An Evolutionarily Conserved Mechanism Delimiting SHR Movement Defines a Single Layer of Endodermis in Plants , 2007, Science.

[25]  Renze Heidstra,et al.  Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action. , 2007, Genes & development.

[26]  Eric Blanc,et al.  Automated structure solution with autoSHARP. , 2007, Methods in molecular biology.

[27]  Randy J. Read,et al.  Phaser crystallographic software , 2007, Journal of applied crystallography.

[28]  Yoshinori Hirano,et al.  Gibberellin-induced DELLA recognition by the gibberellin receptor GID1 , 2008, Nature.

[29]  C. Masuta,et al.  A strategy for screening an inhibitor of viral silencing suppressors, which attenuates symptom development of plant viruses , 2008, FEBS letters.

[30]  A. Muñoz,et al.  GRAS Proteins Form a DNA Binding Complex to Induce Gene Expression during Nodulation Signaling in Medicago truncatula[W] , 2009, The Plant Cell Online.

[31]  Philip N Benfey,et al.  Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. , 2009, The Plant journal : for cell and molecular biology.

[32]  P. Benfey,et al.  Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth , 2010, Nature.

[33]  Randy J. Read,et al.  Acta Crystallographica Section D Biological , 2003 .

[34]  J. Colasanti,et al.  Activity of transcription factor JACKDAW is essential for SHR/SCR-dependent activation of SCARECROW and MAGPIE and is modulated by reciprocal interactions with MAGPIE, SCARECROW and SHORT ROOT , 2011, Plant Molecular Biology.

[35]  E. Rikkerink,et al.  GRAS proteins: the versatile roles of intrinsically disordered proteins in plant signalling. , 2012, The Biochemical journal.

[36]  Randy J. Read,et al.  Phenix - a comprehensive python-based system for macromolecular structure solution , 2012 .

[37]  R. Newcomb,et al.  DAD2 Is an α/β Hydrolase Likely to Be Involved in the Perception of the Plant Branching Hormone, Strigolactone , 2012, Current Biology.

[38]  F. Divol,et al.  Surfing along the root ground tissue gene network. , 2012, Developmental biology.

[39]  Philip N Benfey,et al.  Control of Arabidopsis root development. , 2012, Annual review of plant biology.

[40]  Shinjiro Yamaguchi,et al.  Structures of D14 and D14L in the strigolactone and karrikin signaling pathways , 2013, Genes to cells : devoted to molecular & cellular mechanisms.

[41]  Hongchang Cui,et al.  SCARECROW, SCR-LIKE 23 and SHORT-ROOT control bundle sheath cell fate and function in Arabidopsis thaliana. , 2014, The Plant journal : for cell and molecular biology.

[42]  H. Yoshida,et al.  DELLA protein functions as a transcriptional activator through the DNA binding of the INDETERMINATE DOMAIN family proteins , 2014, Proceedings of the National Academy of Sciences.

[43]  Y. Kamiya,et al.  DELLAs Function as Coactivators of GAI-ASSOCIATED FACTOR1 in Regulation of Gibberellin Homeostasis and Signaling in Arabidopsis[W][OPEN] , 2014, Plant Cell.

[44]  Anna Akhmanova,et al.  Arabidopsis BIRD Zinc Finger Proteins Jointly Stabilize Tissue Boundaries by Confining the Cell Fate Regulator SHORT-ROOT and Contributing to Fate Specification , 2015, Plant Cell.

[45]  Uwe Ohler,et al.  Transcriptional control of tissue formation throughout root development , 2015, Science.

[46]  Qingsong Liu,et al.  Crystal Structure of the GRAS Domain of SCARECROW-LIKE7 in Oryza sativa , 2016, Plant Cell.