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

Abstract

The CBF (C-repeat binding factor) pathway has a major role in plant cold acclimation, the process whereby certain plants increase in freezing tolerance in response to low nonfreezing temperatures. In Arabidopsis thaliana, the pathway is characterized by rapid cold induction of CBF1, CBF2, and CBF3, which encode transcriptional activators, followed by induction of CBF-targeted genes that impart freezing tolerance. At warm temperatures, CBF transcript levels are low, but oscillate due to circadian regulation with peak expression occurring at 8 h after dawn (zeitgeber time 8; ZT8). Here, we establish that the CBF pathway is also regulated by photoperiod at warm temperatures. At ZT8, CBF transcript levels in short-day (SD; 8-h photoperiod) plants were three-to fivefold higher than in long-day plants (LD; 16-h photoperiod). Moreover, the freezing tolerance of SD plants was greater than that of LD plants. Genetic analysis indicated that phytochrome B (PHYB) and two phytochrome-interacting factors, PIF4 and PIF7, act to down-regulate the CBF pathway and freezing tolerance under LD conditions. Down-regulation of the CBF pathway in LD plants correlated with higher PIF4 and PIF7 transcript levels and greater stability of the PIF4 and PIF7 proteins under LD conditions. Our results indicate that during the warm LD growing season, the CBF pathway is actively repressed by PHYB, PIF4, and PIF7, thus mitigating allocation of energy and nutrient resources toward unneeded frost protection. This repression is relieved by shortening day length resulting in up-regulation of the CBF pathway and increased freezing tolerance in preparation for coming cold temperatures.

PIFs: Systems Integrators in Plant Development

“…TOC1, PRR5, and PRR7 also repress PIF4 and PIF5 expression (Yamashino et al, 2003;Niwa et al, 2009). Moreover, PIF7 oscillates in SD, long-day (LD), and free-running conditions, suggesting that expression of PIF7 is probably under clock regulation as well (Kidokoro et al, 2009;Lee and Thomashow, 2012).…”

“…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). The proposed model involves direct transcriptional repression of CBFs by PIF7 and presumably PIF4 during daytime in LDs, which is relieved in SDs through an unknown mechanism that might involve lower accumulation of PIF4 and PIF7 proteins during the day hours compared with LDs (Lee and Thomashow, 2012).…”

“…First, although they appear to represent a minority, a significant number of PIFq-bound genes are upregulated in pif mutants especially during the deetiolation response ( Figure 2C; Oh et al, 2009Oh et al, , 2012Zhang et al, 2013), suggesting that PIFs act as transcriptional repressors of these genes. Second, evidence for PIFs acting as intrinsic transcriptional repressors of specific genes has been provided in a number of cases, such as PIF1 repression of PSY expression in the dark (Toledo-Ortiz et al, 2010), PIF7 repression of CBF2 expression under diurnal conditions (Kidokoro et al, 2009;Lee and Thomashow, 2012), and PIF1 and/or PIF3 repression of genes associated with chlorophyll biosynthesis, photosynthesis, and reactive oxygen species (ROS) responses during deetiolation (Chen et al, 2013;Liu et al, 2013b). Collectively, the data are consistent with a model whereby in environments with low or absent phy activation, PIFs accumulate and either activate the expression of PIF-induced genes or inhibit the expression of PIF-repressed genes, and this activity is rapidly reversed by light through phy-induced degradation of the PIFs (Figures 3A and 3B).…”

Phytochromes and Phytochrome Interacting Factors

“…PIF7 also regulates shade avoidance responses by directly controlling auxin biosynthetic genes under shade conditions (Li et al, 2012a). In addition, PIF7 and PIF4 reduce freezing tolerance responses by directly down-regulating CBF gene expression in a photoperiod-dependent manner (Lee and Thomashow, 2012). Finally, the functional importance of PIF8 is largely unknown; therefore, further efforts are necessary to examine the potential role of PIF8 in light signaling pathways.…”

“…2; Hornitschek et al, 2009;Hao et al, 2012;Lee et al, 2014;Nieto et al, 2015). Besides hypocotyl elongation, PIF4 also controls several physiological and development aspects, such as stomatal development in response to light quality, circadian gating, chlorophyll degradation and leaf senescence in darkness, freezing tolerance, and anthocyanin biosynthesis under red-light conditions Casson et al, 2009;Lee and Thomashow, 2012;Sakuraba et al, 2014;Song et al, 2014;Liu et al, 2015;Zhang et al, 2015;Zhu et al, 2016a).…”