A missense mutation in the glucosamine-6-phosphate N-acetyltransferase-encoding gene causes temperature-dependent growth defects and ectopic lignin deposition in Arabidopsis

Plant Cell. 2012 Aug;24(8):3366-79. doi: 10.1105/tpc.112.102806. Epub 2012 Aug 28.

Abstract

To study the regulatory mechanisms underlying lignin biosynthesis, we isolated and characterized lignescens (lig), a previously undescribed temperature-sensitive mutant of Arabidopsis thaliana that exhibits ectopic lignin deposition and growth defects under high-temperature conditions. The lig mutation was identified as a single base transition in GNA1 encoding glucosamine-6-phosphate N-acetyltransferase (GNA), a critical enzyme of UDP-N-acetylglucosamine (UDP-GlcNAc) biosynthesis. lig harbors a glycine-to-serine substitution at residue 68 (G68S) of GNA1. Enzyme activity assays of the mutant protein (GNA1(G68S)) showed its thermolability relative to the wild-type protein. The lig mutant exposed to the restrictive temperature contained a significantly smaller amount of UDP-GlcNAc than did the wild type. The growth defects and ectopic lignification of lig were suppressed by the addition of UDP-GlcNAc. Since UDP-GlcNAc is an initial sugar donor of N-glycan synthesis and impaired N-glycan synthesis is known to induce the unfolded protein response (UPR), we examined possible relationships between N-glycan synthesis, UPR, and the lig phenotype. N-glycans were reduced and LUMINAL BINDING PROTEIN3, a typical UPR gene, was expressed in lig at the restrictive temperature. Furthermore, treatment with UPR-inducing reagents phenocopied the lig mutant. Our data collectively suggest that impairment of N-glycan synthesis due to a shortage of UDP-GlcNAc leads to ectopic lignin accumulation, mostly through the UPR.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Amino Acid Substitution
  • Arabidopsis / enzymology*
  • Arabidopsis / genetics
  • Arabidopsis / growth & development*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Wall / genetics
  • Cell Wall / metabolism
  • Chromosome Mapping
  • Enzyme Activation
  • Enzyme Assays
  • Enzyme Stability
  • Gene Expression Regulation, Enzymologic
  • Gene Expression Regulation, Plant
  • Genes, Plant
  • Glucosamine / analogs & derivatives
  • Glucosamine 6-Phosphate N-Acetyltransferase / genetics*
  • Glucosamine 6-Phosphate N-Acetyltransferase / metabolism
  • Glucose-6-Phosphate / analogs & derivatives
  • Glycine / metabolism
  • Glycosylation
  • Inbreeding
  • Lignin / biosynthesis*
  • Molecular Sequence Data
  • Mutation, Missense*
  • Phenotype
  • Plant Roots / enzymology
  • Plant Roots / genetics
  • Plant Roots / growth & development
  • Polysaccharides / metabolism
  • Temperature
  • Unfolded Protein Response
  • Uridine Diphosphate N-Acetylglucosamine / metabolism

Substances

  • Arabidopsis Proteins
  • Carrier Proteins
  • Polysaccharides
  • BIP protein, Arabidopsis
  • glucosamine 6-phosphate
  • Uridine Diphosphate N-Acetylglucosamine
  • Glucose-6-Phosphate
  • Lignin
  • Glucosamine 6-Phosphate N-Acetyltransferase
  • Glucosamine
  • Glycine