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

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.

Chloroplast Membrane Remodeling during Freezing Stress Is Accompanied by Cytoplasmic Acidification Activating SENSITIVE TO FREEZING2

“…This enhanced proximity of membranes, lack of fluidity, and low hydration allow nonlamellar structures to form between membranes, fusing subcellular compartments and ultimately resulting in cell death after rehydration (Webb et al, 1994;Uemura et al, 1995). Multiple mechanisms have evolved in plants to avoid both dehydration and membrane fusion, including solute accumulation, cell wall modification, lipid desaturation, and lipid composition changes (Lineberger and Steponkus, 1980;Browse and Xin, 2001;Degenkolbe et al, 2012;Chen and Thelen, 2013;Ji et al, 2015). These changes typically occur during a period of cold acclimation or cold hardening in which plants are exposed to low, nonfreezing temperatures prior to freezing and transcriptional changes accompany increased freezing tolerance.…”

The RCC1 family protein SAB1 negatively regulates ABI5 through multidimensional mechanisms during postgermination in Arabidopsis

“…Three Arabidopsis RCC1 family proteins, UVR8, RUG3 and TCF1, have been functionally characterized, and each of them mediates different biological processes, including UV-B response, tolerance to low temperature and root development (Brown et al, 2005;K€ uhn et al, 2011;Ji et al, 2015). Moreover, these proteins have different subcellular localization: UVR8 is localized in both the nucleus and cytosol, TCF1 is localized in the nucleus and RUG3 is localized in mitochondria (Kaiserli & Jenkins, 2007;K€ uhn et al, 2011;Ji et al, 2015). Here, we show that the RCC1 family protein SAB1 plays a crucial role in ABA-mediated regulation of seed germination and postgerminative growth.…”

“…Histone‐related constructs were described by Ji et al . (). The SAB1 coding region was inserted into pMB150 using BamH I and Sal I sites.…”

“…The SAB1 coding region was cloned in-frame between the EcoRI and Sal I sites of pGBKT7. Histone-related constructs were described by Ji et al (2015). The SAB1 coding region was inserted into pMB150 using BamHI and SalI sites.…”

RUG3 and ATM synergistically regulate the alternative splicing of mitochondrial nad2 and the DNA damage response in Arabidopsis thaliana

“…In plants, there are 24 genes encoding RCC1 family proteins; among them, UVR8 and TCF1 (Tolerant to Chilling and Freezing 1) have been well characterized and both proteins mediate plant response to environmental conditions4546474849. In cells irradiated with ultraviolet B (UVB) light, UVR8 moves from the cytosol to the nucleus, where it activates a signaling cascade that enables the cell to respond to the exposure46.…”