The Arabidopsis RCC1 Family Protein TCF1 Regulates Freezing Tolerance and Cold Acclimation through Modulating Lignin Biosynthesis

PLoS Genet. 2015 Sep 22;11(9):e1005471. doi: 10.1371/journal.pgen.1005471. eCollection 2015.

Abstract

Cell water permeability and cell wall properties are critical to survival of plant cells during freezing, however the underlying molecular mechanisms remain elusive. Here, we report that a specifically cold-induced nuclear protein, Tolerant to Chilling and Freezing 1 (TCF1), interacts with histones H3 and H4 and associates with chromatin containing a target gene, blue-copper-binding protein (BCB), encoding a glycosylphosphatidylinositol-anchored protein that regulates lignin biosynthesis. Loss of TCF1 function leads to reduced BCB transcription through affecting H3K4me2 and H3K27me3 levels within the BCB gene, resulting in reduced lignin content and enhanced freezing tolerance. Furthermore, plants with knocked-down BCB expression (amiRNA-BCB) under cold acclimation had reduced lignin accumulation and increased freezing tolerance. The pal1pal2 double mutant (lignin content reduced by 30% compared with WT) also showed the freezing tolerant phenotype, and TCF1 and BCB act upstream of PALs to regulate lignin content. In addition, TCF1 acts independently of the CBF (C-repeat binding factor) pathway. Our findings delineate a novel molecular pathway linking the TCF1-mediated cold-specific transcriptional program to lignin biosynthesis, thus achieving cell wall remodeling with increased freezing tolerance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acclimatization / genetics*
  • Arabidopsis / genetics*
  • Arabidopsis / physiology
  • Arabidopsis Proteins / biosynthesis
  • Arabidopsis Proteins / genetics*
  • Carrier Proteins / biosynthesis
  • Carrier Proteins / genetics*
  • Cold Temperature
  • Gene Expression Regulation, Plant
  • Gene Knockdown Techniques
  • Histones / genetics
  • Lignin / biosynthesis
  • Lignin / genetics*
  • Nuclear Proteins / genetics*

Substances

  • Arabidopsis Proteins
  • Carrier Proteins
  • Histones
  • Nuclear Proteins
  • TCF1 protein, Arabidopsis
  • copper-binding protein
  • Lignin

Grants and funding

This work was supported by the National Transgenic Key Project of MOA (2014ZX08002-002 to XL), National Science Foundation (31200962 and 31230050) and the Youth Innovation Promotion Association of the Chinese Academy of Sciences. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.