CIRCADIAN CLOCK-ASSOCIATED 1 and LATE ELONGATED HYPOCOTYL regulate expression of the C-REPEAT BINDING FACTOR (CBF) pathway in Arabidopsis

Abstract

The C-REPEAT BINDING FACTOR (CBF) cold-response pathway has a prominent role in cold acclimation, the process whereby certain plants increase tolerance to freezing in response to low nonfreezing temperatures. In Arabidopsis, the CBF pathway is characterized by rapid induction of the C-REPEAT BINDING FACTOR 1 (CBF1), CBF2, and CBF3 genes, which encode transcriptional activators, followed by induction of the CBF-targeted genes known as the "CBF regulon." Expression of the CBF regulon results in an increase in freezing tolerance. Previous studies established that CBF1, CBF2, and CBF3 are subject to circadian regulation and that their cold induction is gated by the circadian clock. Here we present the results of genetic analysis and ChIP experiments indicating that both these forms of regulation involve direct positive action of two transcription factors that are core components of the clock, i.e., CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) and LATE ELON-GATED HYPOCOTYL (LHY). In plants carrying the cca1-11/lhy-21 double mutation, cold induction of CBF1, CBF2, and CBF3 was greatly impaired, and circadian regulation of CBF1 and CBF3 was essentially eliminated; circadian regulation of CBF2 continued, although with significantly reduced amplitude. Circadian regulation and cold induction of three CBF regulon genes, i.e., COLD-REGU-LATED GENE15A (COR15A), COR47, and COR78, also were greatly diminished in plants carrying the cca1-11/lhy-21 double mutation. Furthermore, the cca1-11/lhy-21 double mutation resulted in impaired freezing tolerance in both nonacclimated and cold-acclimated plants. These results indicate that CCA1/LHY-mediated output from the circadian clock contributes to plant cold tolerance through regulation of the CBF cold-response pathway.

Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance inArabidopsis thaliana

“…Given the prominent role of the CBF pathway in cold acclimation, we asked whether the CBF genes were expressed at different levels in SD and LD plants. Previous studies (16,17) established that CBF1, -2, and -3 are regulated by the circadian clock and that the transcript levels for each gene peaks at about 8 h after dawn, a time referred to as zeitgeber time 8 (ZT8). Our results were consistent with these findings; the transcript levels for each CBF gene peaked at about ZT8 under both SD and LD conditions (results for CBF2 are shown in Fig.…”

A DEAD Box RNA Helicase Is Critical for Pre-mRNA Splicing, Cold-Responsive Gene Regulation, and Cold Tolerance inArabidopsis

“…CIR1 is involved in circadian-regulated developmental processes, and circadian rhythmic expression of CIR1 is regulated by the central oscillators CIRCADIAN CLOCK-ASSOCIATED1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), two MYB transcription factors that have partially redundant functions (Schaffer et al, 1998;Wang and Tobin, 1998;Mizoguchi et al, 2002;Zhang et al, 2007). The functions of CCA1 and LHY in the regulation of CBF expression have been reported (Dong et al, 2011), but the function of CIR1 in cold stress response has not been determined. SPFH is one of the SPFH/PHB (stomatin-prohibtin-flotillin-HflC/K) domain-containing superfamily proteins, and members of the SPFH protein superfamily are generally associated with plasma or mitochondrial membranes and are involved in many cellular processes, including protein turnover or oligomerization, cell proliferation, and ion channel regulation (Tavernarakis et al, 1999;Nadimpalli et al, 2000;Rivera-Milla et al, 2006).…”

PIFs: Systems Integrators in Plant Development

“…In the case of cold, the circadian clock regulates the expression and gates the cold induction of the C-repeat binding factors CBF1, 2, and 3, a pathway with a major role in plant cold acclimation and freezing tolerance. The mechanism involves direct CBF induction in the morning by CCA1 and LHY and evening repression by PRR5, 7, and 9 (Dong et al, 2011;Nakamichi et al, 2012). PIF7 and PIF4 also regulate the circadian and diurnal expression of CBFs at warm temperatures, thus potentially participating in the photoperiodic control of the CBF cold acclimation pathway (Kidokoro et al, 2009;Lee and Thomashow, 2012).…”