Cold acclimation by the CBF-COR pathway in a changing climate: Lessons from Arabidopsis thaliana

Abstract

Cold acclimation is a process used by most temperate plants to cope with freezing stress. In this process, the expression of cold-responsive (COR) genes is activated and the genes undergo physiological changes in response to the exposure to low, non-freezing temperatures and other environmental signals. The C-repeat-binding factors (CBFs) have been demonstrated to regulate the expression of many COR genes. Recent studies have elucidated the molecular mechanisms of how plants transmit cold signals from the plasma membrane to the CBFs and the results have indicated that COR genes are also regulated through CBF-independent pathways. Climate change is expected to have a major impact on cold acclimation and freezing tolerance of plants. However, how climate change affects plant cold acclimation at the molecular level remains unclear. This mini-review focuses on recent advances in cold acclimation in Arabidopsis thaliana and discusses how signaling can be potentially impacted by climate change. Understanding how plants acquire cold acclimation is valuable for the improvement of the freezing tolerance in plants and for predicting the effects of climate change on plant distribution and agricultural yield.

Keywords: Abiotic stress; CAMTAs; CBFs; Cold-responsive gene; Local adaptation; Protein kinase.

Fig. 1

Proposed model of signal-induced cold acclimation. Plants acquire cold acclimation through COR gene-dependent and COR gene-independent responses. Acquisition of COR gene expression is categorized into CBF-dependent and CBF-independent pathways. CBFs have been identified as master transcription factors that regulate the expression of many COR genes, including DEAR1, DREB, ZF, CZF2, ZAT10, and AZF2 whose proteins further regulate many COR genes. Expression of HSFC1, ZAT12, and CZF1 is also rapidly induced by cold stress and is involved in the regulation of COR gene expression. Functional redundancy and likely inter-regulation exist among CBF transcription factors. In turn, CBF expression is controlled by other transcription factors, e.g., ICE1, SOC1, MYB15, and CAMTAs. Upstream events include cold-induced calcium influx, enhanced membrane rigidity, activation of protein kinases, and balanced control between protein activation and degradation. These post-translational mechanisms guarantee rapid activation of the CBF transcriptional pathway during cold acclimation and inactivation of the pathway once COR gene expression has been initiated. AZF2 Arabidopsis zinc-finger protein 2, BES1 brassinosteroid-insensitive 1-EMS-suppressor 1, BZR1 brassinazole-resistant 1, CAM Ca²⁺/calmodulin, CAMTAs calmodulin-binding transcription activators, CBF C-repeat binding factor, CCA1 circadian clock-associated 1, CESTA a bHLH transcription factor, COR cold responsive; CRLK1/2, calcium/calmodulin-regulated receptor-like kinases 1 and 2, CRPK1 cold-responsive protein kinase 1, CZF cold-induced zinc-finger protein 2, DEAR1 DREB and EAR motif protein 1, DREB dehydration-responsive element-binding protein, EIN3 ethylene-insensitive 3, HSFC1 heat-shock factor C 1, ICE1 inducer of CBF expression 1, LHY late elongated hypocotyl, MEKK mitogen-activated protein kinase kinase kinase, MKK mitogen-activated protein kinase kinase, MPK mitogen-activated protein kinase, MYB15 MYB transcription factor 15, PIF3/4/7 phytochrome-interacting factor 3, 4 and 7, SOC1 suppressor of constans overexpression 1, ZAT zinc finger of Arabidopsis

Fig. 2

Expression of CBFs regulated by light quality, the circadian clock, and photoperiod. Under warm daytime, a decrease in the R/FR ratio leads to increased CBF expression under long-day or short-day conditions. CCA1 and LHY directly bind to CBF promoters to positively regulate CBF expression in the early morning. PhyB and the activity of PIF4/7 repress CBF expression by directly binding to the promoter region, whereas PIF3 is degraded by EBF1/2. During warm night, CBF expression is inhibited by PRRs and PIF3/4/7. Under short-day conditions, cold stress can occur during the day or night. ICE1 can be activated to induce CBF expression. CAMTA3 and CAMTA5 regulate the expression of CBF1 and CBF2 in response to a rapid temperature decrease. PIF3 represses CBF expression under cold conditions during day and night to balance CBF expression. The expression of CBF is also regulated by chloroplast signals and hormones. CAMTAs calmodulin-binding transcription activators, CBF C-repeat binding factor; CCA1, circadian clock-associated 1, ICE1 inducer of CBF expression 1, LHY late elongated hypocoty l, PIF phytochrome-interacting factor, PRRs pseudo-response regulators, R/FR red to far-red ratio

Fig. 3

Schematic illustration of the impact of climate change on cold acclimation. Cold acclimation is caused by a complex interaction between a decreasing photoperiod and decreases in temperature. Climate change can delay the time of cold acclimation, and cold acclimation will be affected by erratic temperature events. Global warming can directly reduce the effectiveness of cold acclimation by disrupting the combined effects of photoperiod and temperature. Elevated CO₂ concentration affects plant cold acclimation and freezing tolerance by nucleating ice in cells, increasing leaf temperatures, delaying the timing of cold acclimation, and changing xylem sap pH. The increase in leaf temperatures may affect membrane fluidity and the activity of calcium channels, and, thus, subsequent cellular signaling. Changes in xylem sap pH may affect the chemical characters of several COR-gene products and ABA signaling. Elevated CO₂ concentration can affect both the timing and rate of cold acclimation in combination with warmer temperatures, shorter photoperiod, and lower irradiance. CBF C-repeat binding factor, CCA1 circadian clock-associated 1, CO₂ carbon dioxide, LHY late elongated hypocoty l, PhyB phytochrome B, PIF3/4/7 phytochrome-interacting factor 3, 4 and 7, R/FR red to far-red ratio