Gibberellin-induced DELLA recognition by gibberellin receptor GID1. Nature

Structural Biology Laboratory, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0192, Japan.
Nature (Impact Factor: 41.46). 12/2008; 456(7221):459-63. DOI: 10.1038/nature07519
Source: PubMed


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.

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    • "The GA signaling pathway is negatively regulated by DELLA proteins, which contain characteristic DELLA and VHYNP motifs at the N-terminus and the GRAS domain at the C-terminus (Willige et al., 2007). DELLA repression of GA signaling can be relieved through ubiquitin-mediated proteolysis or non-proteolytic GA signaling (Griffiths et al., 2006; Ariizumi et al., 2008; Murase et al., 2008). DELLA genes have been identified in various species , including AtRGA, AtGAI, AtRGL1, AtRGL2, AtRGL3 in Arabidopsis (Lee et al., 2002; Wen and Chang, 2002; Piskurewicz and Lopez-Molina, 2009); SLR1 in rice (Ikeda et al., 2001); and GhRGL, GhSLR1b, GhGAI3a, GhGAI3b, GhGAI4a, GhGAI4b in cotton (Aleman et al., 2008; Liao et al., 2009; Wen et al., 2012). "
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    ABSTRACT: Gibberellins (GA) are some of the most important phytohormones involved in plant development. DELLA proteins are negative regulators of GA signaling in many plants. In this study, the full-length cDNA sequences of three DELLA genes were cloned from Artemisia annua. Phylogenetic analysis revealed that AaDELLA1 and AaDELLA2 were located in the same cluster, but AaDELLA3 was not. Subcellular localization analysis suggested that AaDELLAs can be targeted to the nucleus and/or cytoplasm. Real-time PCR indicated that all three AaDELLA genes exhibited the highest expression in seeds. Expression of all AaDELLA genes was enhanced by exogenous MeJA treatment but inhibited by GA3 treatment. Yeast two-hybrid assay showed that AaDELLAs could interact with basic helix-loop-helix transcription factor AaMYC2, suggesting that GA and JA signaling may be involved in cross-talk via DELLA and MYC2 interaction in A. annua.
    Genetics and molecular research: GMR 09/2015; 14(3):10037-49. DOI:10.4238/2015.August.21.10 · 0.78 Impact Factor
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    • "GA binding to the GID1 receptor stimulates GA responses through the targeted degradation of negative regulators named for the conserved protein motif DELLA (Asp-Glu-Leu-Leu-Ala) (Ueguchi-Tanaka et al. 2005, Ueguchi-Tanaka and Matsuoka 2010, Hauvermale et al. 2012). GA binding causes a conformational change in GID1, resulting in formation of a DELLA-binding surface (Murase et al. 2008, Shimada et al. 2008). The positive regulator of GA responses, SLEEPY1 (SLY1), is the Fbox component of the SCF SLY1 E3 ubiquitin ligase that recognizes the GID1–GA–DELLA complex and ubiquitinates DELLA, thereby targeting it for destruction via the 26S proteasome. "
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    ABSTRACT: Dormancy prevents seeds from germinating under favorable conditions until they have experienced dormancy-breaking conditions, such as after-ripening through a period of dry storage or cold imbibition. Abscisic acid (ABA) hormone signaling establishes and maintains seed dormancy, whereas gibberellin (GA) signaling stimulates germination. ABA levels decrease and GA levels increase with after-ripening and cold stratification. However, increasing GA sensitivity may also be critical to dormancy loss since increasing seed GA levels are detectable only with long periods of after-ripening and imbibition. After-ripening and cold stratification act additively to enhance GA hormone sensitivity in ga1-3 seeds that cannot synthesize GA. Since the overexpression of the GA receptor GID1 (GIBBERELLIN-INSENSITIVE DWARF1) enhanced this dormancy loss, and because gid1a gid1b gid1c triple mutants show decreased germination, the effects of dormancy-breaking treatments on GID1 mRNA and protein accumulation were examined. Partial after-ripening resulted in increased GID1b, but not GID1a or GID1c mRNA levels. Cold imbibition stimulated the accumulation of all three GID1 transcripts, but resulted in no increase in GA sensitivity during ga1-3 seed germination unless seeds were also partially after-ripened. This is probably because after-ripening was needed to enhance GID1 protein accumulation, independently of transcript abundance. The rise in GID1b transcript with after-ripening was not associated with decreased ABA levels, suggesting there is ABA-independent GID1b regulation by after-ripening and the 26S proteasome. GA and the DELLA RGL2 repressor of GA responses differentially regulated the three GID1 transcripts. Moreover, DELLA RGL2 appeared to switch between positive and negative regulation of GID1 expression in response to dormancy-breaking treatments.
    Plant and Cell Physiology 07/2015; 56(9). DOI:10.1093/pcp/pcv084 · 4.93 Impact Factor
    • "Several plant hormone receptors utilize the a/b hydrolase topology to bind bioactive hormone molecules, which causes a conformational change in the protein that is essential for signal relay rather than catalytic activity (Guo et al. 2013; Janssen and Snowden 2012). A good example is the rice gibberellin receptor GID1, in which gibberellin binds to a modified catalytic triad, resulting in a conformational change in the protein, allowing it to connect with the downstream signaling machinery (Murase et al. 2008; Shimada et al. 2008). It is conceivable that PAD4 serine 118 also facilitates a conformational change in PAD4 that impacts defense activity in cells and tissues responding to F. graminearum infection. "
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    ABSTRACT: Fusarium graminearum (Fg) causes Fusarium head blight (FHB) disease in wheat and other cereals. Fg also causes disease in Arabidopsis thaliana. In both Arabidopsis and wheat, Fg infection is limited by salicylic acid (SA) signaling. Here we show that in Arabidopsis, the defense regulator EDS1 (ENHANCED DISEASE SUSCEPTIBILITY1) and its interacting partners, PAD4 (PHYTOALEXIN-DEFICIENT4) and SAG101 (SENESCENCE-ASSOCIATED GENE101) promote SA accumulation to curtail Fg infection. Characterization of plants expressing the PAD4 non-interacting eds1L262P indicated that interaction between EDS1 and PAD4 is critical for defense against Fg. A conserved serine in the predicted acyl hydrolase catalytic triad of PAD4, which is not required for defense against bacterial and oomycete pathogens, is also necessary for limiting Fg infection. These results suggest a molecular configuration of PAD4 in Arabidopsis defense against Fg that is different from its defense contribution against other pathogens. We further show that constitutive expression of Arabidopsis PAD4 can enhance FHB resistance in Arabidopsis and wheat. Taken together with previous studies of wheat and Arabidopsis expressing salicylate hydroxylase or the SA response regulator NPR1 (NON-EXPRESSER OF PR GENES1), our results show that exploring fundamental processes in a model plant provides important leads to manipulating crops for improved disease resistance.
    Molecular Plant-Microbe Interactions 04/2015; 28(8). DOI:10.1094/MPMI-04-15-0079-R · 3.94 Impact Factor
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