O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis

Rodolfo Zentella, Jianhong Hu, Wen Ping Hsieh, Peter A. Matsumoto, Andrew Dawdy, Benjamin Barnhill, Harriëtte Oldenhof, Lynn M. Hartweck, Sushmit Maitra, Stephen G. Thomas, Shelley Cockrell, Michael Boyce, Jeffrey Shabanowitz, Donald F. Hunt, Neil E. Olszewski, Tai Ping Sun

Research output: Contribution to journalArticlepeer-review

89 Scopus citations

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 BRASSINAZOLERESISTANT1 (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.

Original languageEnglish (US)
Pages (from-to)164-176
Number of pages13
JournalGenes and Development
Volume30
Issue number2
DOIs
StatePublished - Jan 15 2016

Bibliographical note

Publisher Copyright:
© 2016 Zentella et al.

Keywords

  • DELLA-interacting proteins
  • Gibberellin signaling
  • Hormone signaling
  • O-GlcNAc transferase
  • O-GlcNAcylation of DELLA
  • SECRET AGENTs

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