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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,  T olerant to  C hilling and  F reezing 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.

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