Arabidopsis O-GlcNAc transferase SEC activates histone methyltransferase ATX1 to regulate flowering

EMBO J. 2018 Oct 1;37(19):e98115. doi: 10.15252/embj.201798115. Epub 2018 Aug 27.

Abstract

Post-translational modification of proteins by O-linked β-N-acetylglucosamine (O-GlcNAc) is catalyzed by O-GlcNAc transferases (OGTs). O-GlcNAc modification of proteins regulates multiple important biological processes in metazoans. However, whether protein O-GlcNAcylation is involved in epigenetic processes during plant development is largely unknown. Here, we show that loss of function of SECRET AGENT (SEC), an OGT in Arabidopsis, leads to an early flowering phenotype. This results from reduced histone H3 lysine 4 trimethylation (H3K4me3) of FLOWERING LOCUS C (FLC) locus, which encodes a key negative regulator of flowering. SEC activates ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1), a histone lysine methyltransferase (HKMT), through O-GlcNAc modification to augment ATX1-mediated H3K4me3 histone modification at FLC locus. SEC transfers an O-GlcNAc group on Ser947 of ATX1, which resides in the SET domain, thereby activating ATX1. Taken together, these results uncover a novel post-translational O-GlcNAc modification-mediated mechanism for regulation of HKMT activity and establish the function of O-GlcNAc signaling in epigenetic processes in plants.

Keywords: SEC; ATX1; HKMT activity; O‐GlcNAcylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Flowers / genetics
  • Flowers / metabolism*
  • Glycosylation
  • Histone Methyltransferases / genetics
  • Histone Methyltransferases / metabolism
  • Histone-Lysine N-Methyltransferase
  • Histones / genetics
  • Histones / metabolism
  • MADS Domain Proteins / genetics
  • MADS Domain Proteins / metabolism
  • Methylation
  • N-Acetylglucosaminyltransferases / genetics
  • N-Acetylglucosaminyltransferases / metabolism*
  • Protein Processing, Post-Translational
  • Signal Transduction / physiology*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • Arabidopsis Proteins
  • FLF protein, Arabidopsis
  • Histones
  • MADS Domain Proteins
  • Transcription Factors
  • Histone Methyltransferases
  • At2g31650 protein, Arabidopsis
  • Histone-Lysine N-Methyltransferase
  • N-Acetylglucosaminyltransferases
  • SECRET AGENT protein, Arabidopsis