title: O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis.
abstract: The DELLA family of transcription regulators functions as master growth repressors in plants by inhibiting phytohormone gibberellin (GA) signaling in response to developmental and environmental cues. DELLAs also play a central role in mediating cross-talk between GA and other signaling pathways via antagonistic direct interactions with key transcription factors. However, how these crucial protein-protein interactions can be dynamically regulated during plant development remains unclear. Here, we show that DELLAs are modified by the O-linked N-acetylglucosamine (O-GlcNAc) transferase (OGT) SECRET AGENT (SEC) in Arabidopsis. O-GlcNAcylation of the DELLA protein REPRESSOR OF ga1-3 (RGA) inhibits RGA binding to four of its interactors-PHYTOCHROME-INTERACTING FACTOR3 (PIF3), PIF4, JASMONATE-ZIM DOMAIN1, and BRASSINAZOLE-RESISTANT1 (BZR1)-that are key regulators in light, jasmonate, and brassinosteroid signaling pathways, respectively. Consistent with this, the sec-null mutant displayed reduced responses to GA and brassinosteroid and showed decreased expression of several common target genes of DELLAs, BZR1, and PIFs. Our results reveal a direct role of OGT in repressing DELLA activity and indicate that O-GlcNAcylation of DELLAs provides a fine-tuning mechanism in coordinating multiple signaling activities during plant development.
authors.affiliation: Department of Biology, Duke University, Durham, North Carolina 27708, USA;
authors.forename: Rodolfo
authors.initials: R
authors.lastname: Zentella
authors.affiliation: Department of Biology, Duke University, Durham, North Carolina 27708, USA;
authors.forename: Jianhong
authors.initials: J
authors.lastname: Hu
authors.affiliation: Department of Biology, Duke University, Durham, North Carolina 27708, USA;
authors.forename: Wen-Ping
authors.initials: WP
authors.lastname: Hsieh
authors.affiliation: Department of Plant Biology, University of Minnesota, Saint Paul, Minnesota 55108, USA;
authors.forename: Peter A
authors.initials: PA
authors.lastname: Matsumoto
authors.affiliation: Department of Chemistry, University of Virginia, Charlottesville, Virginia 22901, USA;
authors.forename: Andrew
authors.initials: A
authors.lastname: Dawdy
authors.affiliation: Department of Chemistry, University of Virginia, Charlottesville, Virginia 22901, USA;
authors.forename: Benjamin
authors.initials: B
authors.lastname: Barnhill
authors.affiliation: Department of Plant Biology, University of Minnesota, Saint Paul, Minnesota 55108, USA;
authors.forename: Harriëtte
authors.initials: H
authors.lastname: Oldenhof
authors.affiliation: Department of Plant Biology, University of Minnesota, Saint Paul, Minnesota 55108, USA;
authors.forename: Lynn M
authors.initials: LM
authors.lastname: Hartweck
authors.affiliation: Department of Chemistry, University of Virginia, Charlottesville, Virginia 22901, USA;
authors.forename: Sushmit
authors.initials: S
authors.lastname: Maitra
authors.affiliation: Department of Biology, Duke University, Durham, North Carolina 27708, USA;
authors.forename: Stephen G
authors.initials: SG
authors.lastname: Thomas
authors.affiliation: Department of Biology, Duke University, Durham, North Carolina 27708, USA;
authors.forename: Shelley
authors.initials: S
authors.lastname: Cockrell
authors.affiliation: Department of Biochemistry, Duke University School of Medicine, Durham, North Carolina 27710, USA;
authors.forename: Michael
authors.initials: M
authors.lastname: Boyce
authors.affiliation: Department of Chemistry, University of Virginia, Charlottesville, Virginia 22901, USA;
authors.forename: Jeffrey
authors.initials: J
authors.lastname: Shabanowitz
authors.affiliation: Department of Chemistry, University of Virginia, Charlottesville, Virginia 22901, USA; Department of Pathology, University of Virginia, Charlottesville, Virginia 22901, USA.
authors.forename: Donald F
authors.initials: DF
authors.lastname: Hunt
authors.affiliation: Department of Plant Biology, University of Minnesota, Saint Paul, Minnesota 55108, USA;
authors.forename: Neil E
authors.initials: NE
authors.lastname: Olszewski
authors.affiliation: Department of Biology, Duke University, Durham, North Carolina 27708, USA;
authors.forename: Tai-Ping
authors.initials: TP
authors.lastname: Sun
mesh_terms: D000215:Acylation; D017360:Arabidopsis / Q000254:growth & development / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant / Q000235:genetics*; D005875:Gibberellins / Q000378:metabolism; D009154:Mutation; D017351:N-Acetylglucosaminyltransferases / Q000235:genetics / Q000378:metabolism*; D011485:Protein Binding; D015398:Signal Transduction / Q000502:physiology*
chemical_list: D029681:Arabidopsis Proteins; C109555:GAI protein, Arabidopsis; D005875:Gibberellins; D017351:N-Acetylglucosaminyltransferases; C510668:SECRET AGENT protein, Arabidopsis
keywords: DELLA-interacting proteins; O-GlcNAc transferase; O-GlcNAcylation of DELLA; SECRET AGENT; gibberellin signaling; hormone signaling