Gibberellin-induced DELLA recognition by the gibberellin receptor GID1

Gibberellins control a range of growth and developmental processes in higher plants and have been widely used in the agricultural industry. By binding to a nuclear receptor, GIBBERELLIN INSENSITIVE DWARF1 (GID1), gibberellins regulate gene expression by promoting degradation of the transcriptional regulator DELLA proteins, including GIBBERELLIN INSENSITIVE (GAI). The precise manner in which GID1 discriminates and becomes activated by bioactive gibberellins for specific binding to DELLA proteins remains unclear. Here we present the crystal structure of a ternary complex of Arabidopsis thaliana GID1A, a bioactive gibberellin and the amino-terminal DELLA domain of GAI. In this complex, GID1A occludes gibberellin in a deep binding pocket covered by its N-terminal helical switch region, which in turn interacts with the DELLA domain containing DELLA, VHYNP and LExLE motifs. Our results establish a structural model of a plant hormone receptor that is distinct from the mechanism of the hormone perception and effector recognition of the known auxin receptors.

[1]  J. Peng,et al.  The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. , 1997, Genes & development.

[2]  J. Macmillan.  Occurrence of Gibberellins in Vascular Plants, Fungi, and Bacteria , 2001, Journal of Plant Growth Regulation.

[3]  M. Talón,et al.  Endogenous gibberellins in Arabidopsis thaliana and possible steps blocked in the biosynthetic pathways of the semidwarf ga4 and ga5 mutants. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[4]  T. Sun,et al.  The DELLA motif is essential for gibberellin-induced degradation of RGA , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[5]  T. Kuromori,et al.  Multiple loss-of-function of Arabidopsis gibberellin receptor AtGID1s completely shuts down a gibberellin signal. , 2007, The Plant journal : for cell and molecular biology.

[6]  T. Yabuta.  On the crystal of gibberellin, a substance to promote plant growth. , 1938 .

[7]  C. Schwechheimer,et al.  The DELLA Domain of GA INSENSITIVE Mediates the Interaction with the GA INSENSITIVE DWARF1A Gibberellin Receptor of Arabidopsis[W] , 2007, The Plant Cell Online.

[8]  Zhong-Lin Zhang,et al.  Genetic Characterization and Functional Analysis of the GID1 Gibberellin Receptors in Arabidopsis[W] , 2006, The Plant Cell Online.

[9]  T. Sun,et al.  Repressing a Repressor , 2001, The Plant Cell Online.

[10]  M. Weiner,et al.  Site-directed mutagenesis of double-stranded DNA by the polymerase chain reaction. , 1994, Gene.

[11]  F. Crick,et al.  The packing of α‐helices: simple coiled‐coils , 1953 .

[12]  Shinjiro Yamaguchi,et al.  Gibberellin metabolism and its regulation. , 2008, Annual review of plant biology.

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

[14]  Masatomo Kobayashi,et al.  GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin , 2005, Nature.

[15]  Thomas Terwilliger,et al.  SOLVE and RESOLVE: automated structure solution, density modification and model building. , 2004, Journal of synchrotron radiation.

[16]  F. Richards,et al.  1H-15N heteronuclear NMR studies of Escherichia coli thioredoxin in samples isotopically labeled by residue type. , 1985, Biochemistry.

[17]  Jack Snoeyink,et al.  Nucleic Acids Research Advance Access published April 22, 2007 MolProbity: all-atom contacts and structure validation for proteins and nucleic acids , 2007 .

[18]  Edward N Baker,et al.  High-resolution crystal structure of plant carboxylesterase AeCXE1, from Actinidia eriantha, and its complex with a high-affinity inhibitor paraoxon. , 2007, Biochemistry.

[19]  M. Estelle,et al.  The F-box protein TIR1 is an auxin receptor , 2005, Nature.

[20]  C. Chien,et al.  The utility F-box for protein destruction , 2008, Cellular and Molecular Life Sciences.

[21]  J. Davies,et al.  Molecular Biology of the Cell , 1983, Bristol Medico-Chirurgical Journal.

[22]  M. Matsuoka,et al.  The Gibberellin Signaling Pathway Is Regulated by the Appearance and Disappearance of SLENDER RICE1 in Nuclei Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010319. , 2002, The Plant Cell Online.

[23]  J. Noel,et al.  Methylation of Gibberellins by Arabidopsis GAMT1 and GAMT2[W] , 2007, The Plant Cell Online.

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

[25]  Bryan C Thines,et al.  JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling , 2007, Nature.

[26]  T. Sun,et al.  Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. , 2001, Genetics.

[27]  Jinrong Peng,et al.  Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. , 2002, Genes & development.

[28]  P. Hedden,et al.  Molecular cloning and functional expression of gibberellin 2- oxidases, multifunctional enzymes involved in gibberellin deactivation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[29]  C. M. Karssen,et al.  Gibberellins in seeds of Arabidopsis thaliana: biological activities, identification and effects of light and chilling on endogenous levels , 1994, Plant Growth Regulation.

[30]  Ottoline Leyser,et al.  The Arabidopsis F-box protein TIR1 is an auxin receptor , 2005, Nature.

[31]  K. Asano,et al.  Molecular Interactions of a Soluble Gibberellin Receptor, GID1, with a Rice DELLA Protein, SLR1, and Gibberellin[W] , 2007, The Plant Cell Online.

[32]  Xiangdong Fu,et al.  The Arabidopsis Mutant sleepy1gar2-1 Protein Promotes Plant Growth by Increasing the Affinity of the SCFSLY1 E3 Ubiquitin Ligase for DELLA Protein Substrates , 2004, The Plant Cell Online.

[33]  Thomas C Terwilliger,et al.  Automated structure solution, density modification and model building. , 2002, Acta crystallographica. Section D, Biological crystallography.

[34]  T. Sun,et al.  The Arabidopsis RGA Gene Encodes a Transcriptional Regulator Repressing the Gibberellin Signal Transduction Pathway , 1998, Plant Cell.

[35]  M. Radley.  Occurrence of Substances Similar to Gibberellic Acid in Higher Plants , 1956, Nature.

[36]  T. Sun,et al.  The Arabidopsis SLEEPY1 Gene Encodes a Putative F-Box Subunit of an SCF E3 Ubiquitin Ligase Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010827. , 2003, The Plant Cell Online.

[37]  R J Read,et al.  Crystallography & NMR system: A new software suite for macromolecular structure determination. , 1998, Acta crystallographica. Section D, Biological crystallography.

[38]  Yunde Zhao,et al.  Plant hormones and signaling: common themes and new developments. , 2008, Developmental cell.

[39]  S. Iuchi,et al.  Identification and characterization of Arabidopsis gibberellin receptors. , 2006, The Plant journal : for cell and molecular biology.

[40]  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.

[41]  T. Moritz,et al.  Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. , 2001, Genetics.

[42]  J. Ecker,et al.  DELLA Proteins and Gibberellin-Regulated Seed Germination and Floral Development in Arabidopsis1[w] , 2004, Plant Physiology.

[43]  Yuji Kamiya,et al.  Global Analysis of DELLA Direct Targets in Early Gibberellin Signaling in Arabidopsis[W] , 2007, The Plant Cell Online.

[44]  David Neil Cooper,et al.  Nature encyclopedia of the human genome , 2003 .

[45]  J. Micol,et al.  The JAZ family of repressors is the missing link in jasmonate signalling , 2007, Nature.

[46]  T. Sun,et al.  The Arabidopsis F-Box Protein SLEEPY1 Targets Gibberellin Signaling Repressors for Gibberellin-Induced Degradation , 2004, The Plant Cell Online.

[47]  Robert H. Blessing,et al.  Towards automated protein structure determination: BnP, the SnB-PHASES interface , 2002 .

[48]  D. Luo,et al.  Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function , 2004, Development.

[49]  G. Johnson,et al.  Nature Encyclopedia of the Human Genome , 2004 .

[50]  Michal Sharon,et al.  Mechanism of auxin perception by the TIR1 ubiquitin ligase , 2007, Nature.

[51]  Masatomo Kobayashi,et al.  Accumulation of Phosphorylated Repressor for Gibberellin Signaling in an F-box Mutant , 2003, Science.