Skip to main content
PMC home page
Springer logoLink to Springer
. 2019 Jan 16;38(5):511–519. doi: 10.1007/s00299-019-02376-3

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

Yukun Liu 1,✉, Peiyu Dang 1, Lixia Liu 2, Chengzhong He 3,✉
PMCID: PMC6488690  PMID: 30652229

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: CBFs, CAMTAs, Protein kinase, Cold-responsive gene, Abiotic stress, Local adaptation

Introduction

Cold temperature (chilling or freezing) is a recurring phenomenon that limits the geographical distribution and agricultural yield of plants. Cold exerts adverse effects on most plant species and causes cold stress. Over the course of their evolutionary history, plants developed different strategies to adapt to cold stress (Korner 2016). Most freezing-tolerant plants acquire this ability via cold acclimation, through exposure to low temperatures that remain above freezing (Thomashow 1999). Experimental studies showed that acquisition of cold acclimation requires the orchestration of transcriptional, biochemical, and physiological changes. During cold acclimation, C-repeat binding factors (CBFs) activate cold-responsive (COR) genes and subsequent accumulation of cryoprotectants, which results in the acquisition of freezing tolerance (Thomashow 1999). Under natural conditions, cold acclimation is a plant response that ensures seasonal survive of low winter temperatures. Cold acclimation, often associated with decreasing photoperiod, initiates the cessation of tree growth in winter and freezing tolerance (Maurya and Bhalerao 2017). Climate change causes rapid temperature changes combined with increasing atmospheric CO2 concentrations (Shepherd 2016), which impacts plant cold acclimation and freezing tolerance. This review focuses on how the cold signal is sensed and transduced into the nucleus and the potential impact of climate change on plant cold acclimation is discussed.

Regulation of COR genes by CBF-dependent and CBF-independent pathways

Overall, cold acclimation is a result of both COR gene-dependent and COR gene-independent responses. Expression of COR genes can be regulated through CBF-dependent and CBF-independent pathways (Fig. 1). COR genes are rapidly induced (ranging from minutes to several hours) by low temperature during cold acclimation (Thomashow 1999). Many products of the COR genes have been suggested to function in the acquisition of cold acclimation and subsequent freezing tolerance. These products include enzymes to biosynthesize osmo-protectants, late embryogenesis abundant proteins, transcription factors, protein kinases, proteins associated with lipid metabolism, proteins for hormone responses, cell wall modifiers, and chloroplast proteins. A 24-h treatment at 4 °C induces about 4000 COR genes in Arabidopsis thaliana (Zhao et al. 2016). CBF1, CBF2, and CBF3 (also known as DREB1b, DREB1c, and DREB1a, respectively; Kidokoro et al. 2017) regulate about 10% of all COR genes (Park et al. 2015). It has been shown that the genes induced or repressed by each CBF are very similar, suggesting that the three CBF proteins are partly redundant in regulating the COR genes (Park et al. 2015; Jia et al. 2016; Zhao et al. 2016; Shi et al. 2017). However, distinct functions of CBFs have also been reported, indicated by the differential expression patterns of the CBF genes during cold acclimation (Shi et al. 2017).

Fig. 1.

Fig. 1

Open in a new tab

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

The CBF proteins directly regulate COR genes by the CCGAC cis-acting element known as the C-repeat (CRT)/dehydration-responsive element (Thomashow 1999). However, not all CBF-regulated COR genes are directly regulated by CBF proteins. Analysis of the promoters of the CBF-activated COR genes in A. thaliana showed that about 38% have no CRT in the 1000 bp upstream of the ATG start codon (Zhao et al. 2016). Furthermore, expression of few CBF-regulated COR genes with or without CRT is repressed, indicating that more transcription factors are involved in the regulation of CBF-regulated COR genes. In addition to CBFs, expression of the other 27 first-wave (rapidly induced in parallel with CBFs) transcription factors are also induced during cold acclimation in A. thaliana (Vogel et al. 2005; Park et al. 2015; Zhao et al. 2016). Six of them (DEAR1, DREB, ZF, CZF2, ZAT10, and AZF2) are significantly repressed in the cbf1/2/3 triple mutant, indicating that the cold-induced expression of these genes is CBF dependent (Zhao et al. 2016). The functions of ZF and ZAT10 were tested via transgenic expression. Overexpression of each induces the expression of COR genes even without cold treatment, suggesting that their transcriptional activities are involved in regulating COR genes (Park et al. 2015; Zhao et al. 2016).

The CBF-independent pathway is involved in the regulation of COR genes, as not all COR genes are affected by CBF genes (i.e., in single, double, or triple cbf mutants of A. thaliana). Among the 27 first-wave transcription factors, HSFC1, ZAT12, and CZF1 regulate the expression of COR genes, but their expression is not affected in cbf triple mutants (Park et al. 2015; Jia et al. 2016; Zhao et al. 2016; Shi et al. 2017). Since only 11 of the 27 first-wave transcription factors have been tested, it is possible that additional CBF-independent transcription factors are involved in the regulation of COR gene expression.

The COR gene expression is complex because two or more first-wave transcription factors share common downstream genes (Park et al. 2015; Zhao et al. 2016). The regulatory network of COR genes is highly interconnected and involves both extensive crosstalk and co-regulation. The regulatory network extends to genes encoding the transcription factors themselves, e.g., CBF2 regulates the expression of ZF, HSFC1 regulates the expression of ZAT12, and CZF1 regulates the expression of ZAT10 (Park et al. 2015; Zhao et al. 2016). Therefore, it seems that cold acclimation is orchestrated by several master proteins and facilitated by other transcription factors, where a coordinated signaling and regulatory network leads to rapid changes of transcriptome.

Expression and regulation of CBF genes

In cold acclimation, the CBF-dependent pathway has been recognized as key to regulate the expression of many COR genes. In turn, CBFs can also be rapidly induced by low temperature during cold acclimation (Thomashow 1999). CBFs have been identified as a gene family in plants and cold induces different expression patterns of different CBF members with regard to specific expression and kinetics (Tondelli et al. 2011). In addition, the expression of CBFs is regulated by light quality, the circadian clock, and photoperiod under normal (e.g., 22 °C) temperatures. Cold-induced CBF expression can be affected by light quality, the circadian clock, and photoperiod. The phytochrome-interacting factor 3/4/7 (PIF3/4/7) directly binds to CBF promoters in A. thaliana and negatively regulate CBF expression, whereas circadian clock-associated 1 (CCA1) and late elongated hypocotyl (LHY) directly bind to CBF promoters and positively regulate CBF expression (Kidokoro et al. 2009; Dong et al. 2011; Lee and Thomashow 2012; Jiang et al. 2017). During cold acclimation, pseudo-response regulator 5/7/9 (PRR5/7/9) is implicated in repressing CBF expression by affecting the expression of CCA1 and LHY (Nakamichi et al. 2009). The decrease in the red to far-red (R/FR) ratio increases CBF expression (Franklin and Whitelam 2007). COR27 and COR28 are nighttime repressors (Wang et al. 2017). Blue light-repressed COR27 and COR28 have been shown to negatively regulate CBF expression through crosstalk with CCA1 function and with PRR5 expression via unknown mechanisms (Li et al. 2016). Recent studies reported that circadian regulation of CBF expression includes plastid signals. LONG HYPOCOTYL 5 (HY5) and PRR5 repress basal expression of CBFs. Specifically, HY5 represses the expression of CBF3. The molecular chaperone HSP90 directly controls the F-box protein ZEITLUPE (ZTL) to negatively regulate HY5 and PRR5. In turn, the heat-shock protein 90 (HSP90)–ZTL complex is negatively regulated by a plastid signal triggered by tetrapyrrole accumulation, providing a signaling cascade that regulates nuclear expression of CBF genes using tetrapyrrole accumulation (Noren et al. 2016).

During cold acclimation, several transcription factors have been identified to regulate the expression of CBFs by binding to their promoters. In A. thaliana, inducer of CBF expression 1 (ICE1) is an MYC-like basic helix–loop–helix transcription factor that binds to the MYC cis-acting elements in the CBF promoter (Chinnusamy et al. 2003; Ding et al. 2015; Kim et al. 2015). The function of ICE1 depends on its post-translational modification but not gene expression (Chinnusamy et al. 2003; Miura et al. 2007, 2011; Ding et al. 2015, 2018). Recent reports showed that ICE1 is regulated by mitogen-activated protein kinase (MPK) signaling cascades that typically comprise three protein kinases: MEKK, MKK, and MPK, which act in series (i.e., MEKK–MKK–MPK; Liu 2012; Liu and He 2017). The MKK4/5–MPK3/6 pathway promotes degradation of ICE1 and repression of CBF genes (Li et al. 2017; Zhao et al. 2017). During cold acclimation, the cold signal causes calcium influx that activates calcium/calmodulin-regulated receptor-like kinases 1 and 2 (CRLK1/2) on the plasma membrane (Yang et al. 2010; Zhao et al. 2017). CRLK1 and CRLK2 initiate a MEKK1–MKK1/2–MPK4 cascade to antagonize the MKK4/5–MPK3/6 pathway, leading to activation of ICE1 and expression of CBF genes (Li et al. 2017; Zhao et al. 2017). Accordingly, CBF proteins regulate the expression of COR genes and generate cryoprotectants, resulting in the acquisition of freezing tolerance. Activation of the MPK3/6 pathway is likely restricted to the cytosol during the early stages, whereas it promotes degradation of ICE1 in the nucleus at a later stage (Liu and Zhou 2018). These studies have proposed a model to account for how plants transmit a cold signal from the plasma membrane to the CBF-regulated COR genes during cold acclimation. Furthermore, MYB15 is a cold-inducible transcription factor and its transcriptional activity peaks after that of CBFs. MYB15 represses expression of the CBFs by directly binding to MYB recognition sites in CBF1, CBF2, and CBF3 promoters (Agarwal et al. 2006). It is also possible that MAPK signaling regulates the MYB15 protein, suggesting a regulatory network upstream of CBFs during cold acclimation (Kim et al. 2017a). In addition, activation of cold-responsive protein kinase 1(CRPK1) occurs on the plasma membrane. CRPK1 phosphorylates 14-3-3 proteins that represent a family of highly conserved regulatory proteins in eukaryotes. In A. thaliana, phosphorylation of the κ and λ isoforms of 14-3-3 proteins promotes their shuttle from the cytosol to the nucleus, where they interact with and destabilize CBF proteins (Liu et al. 2017).

Calmodulin binding transcription activator (CAMTA) transcription factors are positive regulators of CBFs (Doherty et al. 2009). CAMTA1, CAMTA2, CAMTA3, and CAMTA5 induce expression of the CBFs within minutes in response to low temperature. CAMTA1, CAMTA2, CAMTA3, and CAMTA5 have been reported to directly bind to the CBF2 promoter (Doherty et al. 2009; Kim et al. 2013; Kidokoro et al. 2017). However, the camta3 mutations alone, as well as camta1, camta2, camta4, camta5, and camta6 alone, do not show reduced freezing tolerance compared to wild type, indicating that cold acclimation requires the combined function of at least two members of the CAMTA family (Doherty et al. 2009; Kidokoro et al. 2017). Under natural conditions, low temperature can either occur as a sudden temperature drop (e.g., cold shock during the night or under abnormal weather conditions) or as a gradual temperature decrease (e.g., temperature change from autumn to winter). Although the expression of CBF and COR genes occurs during both rapid and gradual temperature decreases, different signaling pathways may be involved. Recent studies indicated that CAMTA3 and CAMTA5 regulate the expression of CBF1 and CBF2 during the day and night in response to a rapid but not slow temperature decrease, suggesting that CAMTA3 and CAMTA5 may function in cold shock signaling but not in the temperature change from autumn to winter (Kidokoro et al. 2017). The activation mechanisms of CAMTAs and how they interconnect with circadian regulation of CBFs during cold acclimation requires further study.

CBF–COR pathway functions in other plants than A. thaliana

CBF genes have been identified in a range of plant species, ranging from grasses to trees (Puhakainen et al. 2004; Benedict et al. 2006; Tondelli et al. 2011). The initiation of cold acclimation in trees involves extensive reprogramming of gene expression that has been reported to include functional CBF genes (Puhakainen et al. 2004; Benedict et al. 2006; Welling and Palva 2008; Menon et al. 2015). For instance, in poplar, PtCBF1, PtCBF2, PtCBF3, and PtCBF4 are induced at 5 °C in leaves, whereas only PtCBF1 and PtCBF3 show significant induction in stems. In leaves, PtCBF1 and PtCBF2 transcript levels peak 8 h after transfer to 5 °C, and PtCBF3 and PtCBF4 transcript levels peak at 3 h (Benedict et al. 2006). Overexpression of a CBF gene from A. thaliana in other plant species or overexpression of CBFs from other species in A. thaliana confers increased freezing tolerance. It also induces expression of CBF-regulated COR genes, indicating that the function of CBF genes is widely conserved in higher plants (Benedict et al. 2006; Tondelli et al. 2011). Furthermore, overexpression of a CBF gene, e.g., in apple, barley, potato, and poplar, enhances freezing tolerance even without cold acclimation. The enhanced freezing tolerance in transgenic plants is accompanied by the induction of COR genes (Benedict et al. 2006; Pino et al. 2008; Wisniewski et al. 2011; Jeknic et al. 2014; Soltesz et al. 2013; Park et al. 2015). In birch and poplar, freezing tolerance is reached after several weeks of cold acclimation in which CBF genes are affected by both photoperiod and day/night temperature cycling, indicating that CBF genes are functional in cold acclimation under natural conditions (Puhakainen et al. 2004; Welling and Palva 2008). However, the initiation of cold acclimation under natural conditions and responses by plants for the survive of seasonally low winter temperatures are complex and the key function of the CBF–COR pathway in these processes requires further study.

Potential impact of climate change on signal transduction of cold acclimation

Under natural autumn conditions, most temperate plants acquire cold acclimation by detecting the complex interaction between decreasing photoperiod and decreasing temperature (Rapacz et al. 2014; Maurya and Bhalerao 2017). Both timing and rate of cold acclimation are critical for freezing tolerance and successful overwintering. The expression of CBF genes is affected by both light quality and photoperiod (Fig. 2). With increasing temperature, cold acclimation will occur later in autumn or early winter with shorter photoperiods and lower total irradiance. Therefore, global warming can directly reduce the effectiveness of cold acclimation by disrupting the combined effects of photoperiod and temperature (Fig. 3). Indeed, at high latitudes, freezing tolerance of perennial grasses is impaired when cold acclimation occurs during warmer extended autumns (Dalmannsdottir et al. 2017). Another feature of temperature change in a changing climate is the frequency and severity of erratic temperature events. Disorganized cold acclimation causes higher susceptibility of plants to erratic temperature events. Erratic temperatures affect the plant freezing tolerance is mainly through deacclimation and reacclimation, two processes that also include expressions of COR genes and CBF genes (Kovi et al. 2016; Pagter and Arora 2013).

Fig. 2.

Fig. 2

Open in a new tab

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.

Fig. 3

Open in a new tab

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

Cold acclimation is correlated to the ability to resist pathogens. At warmer temperatures (22 °C), CAMTA3 inhibits salicylic acid (SA)-mediated immunity in healthy plants. During cold acclimation, however, repression of the SA immunity by CAMTA3 can be overcome (Kim et al. 2013, 2017b). Therefore, CAMTA3-mediated cold acclimation not only contributes to subsequent freezing tolerance but also to SA-mediated immunity. Later in autumn, global warming disrupts cold acclimation and also cold acclimation-associated plant immunity. Since global warming favors survival of pathogens later in autumn (Newton et al. 2012), climate change can ultimately expand the opportunities for disease outbreak in particular plant species.

Elevated CO2 levels increase leaf temperatures mainly due to CO2-induced decrease in stomatal conductance during the day (Fig. 3; Ruiz-Vera et al. 2015). The increase in leaf temperature affects membrane fluidity and the activity of calcium channels that have been shown to activate CRLK1/2 and downstream MAPK signaling (Fig. 1). Elevated CO2 has been suggested to change xylem sap pH, which affects the chemical characteristics of several COR-gene products (Fig. 3). Changes in xylem sap pH have been suggested to increase ABA, which plays a role in the development of freeze tolerance (Eremina et al. 2016). Furthermore, the profound effect of elevated CO2 on cold acclimation originates from its combined effect with warmer temperature, shorter photoperiod, and lower irradiance (Fig. 3). Elevated temperature and CO2 during autumn and a shorter photoperiod have been reported to stimulate late-season net photosynthesis while impairing freezing tolerance in Pinus strobus seedlings (Chang et al. 2016).

Climate change affects the geographical plant distribution. The CBF pathway has been shown to be involved in local adaptation in A. thaliana during evolution. Analyses indicated that accessions collected from relatively warm environments express lower levels of CBF genes and downstream COR genes following cold acclimation compared to accessions from relatively lower winter temperature environments (Zhen and Ungerer 2008; Kang et al. 2013; Gehan et al. 2015). This difference occurs because southern accessions harbor more singletons in the promoter and coding regions of CBF genes. Long-term repression of the CBF pathway in climatic regions where plants experience low temperatures but not freezing stress might be advantageous and provide a driver for selection, as it has been shown that CBFs delay plant growth (Achard et al. 2008; Park et al. 2015). It seems that there is a trade-off of allocation of energy and nutrient resource allocation between plant growth and freezing tolerance (Hoermiller et al. 2017).

The CBF genes have been identified in numerous temperate plant taxa (Puhakainen et al. 2004; Benedict et al. 2006; Tondelli et al. 2011; Guo et al. 2018; Shi et al. 2018). In each particular plant species, at least one CBF gene can be induced in response to low temperature. However, despite conservation of CBF genes, plants do not show the same acquisition of freezing tolerance after cold acclimation. Overall, defective functioning of the CBF pathway could evolve through a mutation in the promoter (affecting CBF expression) or a mutation in a coding region (affecting binding of CBF to promoters of COR genes or affecting CBF stability). Therefore, cold responses in plants that do not acclimate to the cold are not strictly related to the expression of CBF genes. The CBF pathway has been reported to be involved in local adaptation in Arabidopsis during evolution. Analyses have indicated that accessions collected from relatively warm environments express lower levels of CBF genes and downstream COR genes following cold acclimation when compared to accessions from relatively lower winter temperature environments (Zhen and Ungerer 2008; Kang et al. 2013; Gehan et al. 2015). This difference may occur because the southern accessions harbor more singletons in the promoter and coding regions of the CBF genes. Long-term repression of the CBF pathway in climatic regions where plants might experience low temperatures but not freezing stress might be advantageous and provide a driver for selection, as it has been shown that CBFs retard plant growth (Achard et al. 2008; Park et al. 2015). Recent studies revealed a trade-off of allocation of energy and nutrient resources between plant growth and freezing tolerance (Hoermiller et al. 2017). Further studies are expected to investigate whether divergence in the CBF gene family among populations of other than A. thaliana plays an important role in the adaptive variation of cold acclimation in different geographic regions. Studies on the CBF pathway will have important implications for the expansion of plant ranges, invasiveness, and adaptation to novel climates.

Conclusion and future perspectives

Cold is a major abiotic factor that affects plant growth, development, and survival on a daily and seasonal basis. The effects become more complicated due to the impact of climate change. Plants acquire freezing tolerance by cold acclimation, indicating that cold stress is perceived by plant cells. Recent studies reported the function of MAPK–ICE1 signaling in the regulation of CBFs (Fig. 1). Nevertheless, ICE1 is just one of the regulators of CBF genes. The elaborate mechanisms and possible regulatory networks upstream of the expression of CBF genes require further investigation. Furthermore, since the expression of CBFs is regulated by light quality, the circadian clock, and photoperiod (Fig. 2), understanding the daily and seasonal regulation of CBFs is necessary. In addition, COR gene expression is regulated by CBF-independent pathways and cold acclimation depends on COR gene-independent responses. Descriptions of the COR gene-independent responses and CBF-independent expression of COR genes are rare and further work is required.

Although CBF-dependent signaling has been demonstrated to be the major pathway to regulate the expression of COR genes, COR gene expression is also regulated by CBF-independent pathways. Furthermore, cold acclimation also depends on COR gene-independent responses (Fig. 1). Descriptions of the COR gene-independent responses and CBF-independent expression of COR genes are scarce and further responses should be documented. Moreover, it has been revealed that organelles and possibly the vacuole can also sense cold signals to modulate cellular metabolism and the proteome composition (Moellering et al. 2010). In addition, signaling transduction during cold acclimation is made even more complex by retrograde signals, whereby gene expression in the nucleus, chloroplast, and mitochondria must be coordinated depending on the status of the cell as a whole. Further studies are required to reveal the mechanisms of organelles and retrograde signaling during cold acclimation.

Due to increasing global temperatures in association with increasing atmospheric concentrations of CO2, future winters are expected to be milder. However, this change seems to harm plants as it disrupts cold acclimation and freezing tolerance (Fig. 3). Climate change can affect cold acclimation through the CBF–COR signaling pathway. Natural variation during cold acclimation has been shown to be associated with the geographical distribution of plants. Plants in climatic regions with low temperatures but not freezing stress tend to have evolved a defectively functioning CBF pathway, indicating that the CBF pathway is involved in local adaptation. More studies are required to measure the impact of climate change on cold acclimation at the molecular level. Although many questions remain unanswered, further research will expand our understanding of the signal transduction and regulation underlying cold acclimation in plants.

Author contribution statement

YL and CH conceived and designed the review. YL, PD, and LL wrote the manuscript. All authors read and approved the manuscript.

Acknowledgements

Our work was supported by the Nation Natural Science Foundation of China (No. 31560198 and No. 31360166) and the Natural Science Foundation of Shandong Province (No. ZR2013CL005).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Footnotes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Yukun Liu, Phone: +86-871-63862042, Email: ykliu@swfu.edu.cn.

Chengzhong He, Phone: +86-871-63863213, Email: hcz70@163.com.

References

  1. Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P. The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell. 2008;20:2117–2129. doi: 10.1105/tpc.108.058941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, et al. A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem. 2006;281:37636–37645. doi: 10.1074/jbc.M605895200. [DOI] [PubMed] [Google Scholar]
  3. Benedict C, Skinner JS, Meng R, Chang Y, Bhalerao R, Huner NP, et al. The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Plant Cell Environ. 2006;29:1259–1272. doi: 10.1111/j.1365-3040.2006.01505.x. [DOI] [PubMed] [Google Scholar]
  4. Chang CY, Frechette E, Unda F, Mansfield SD, Ensminger I. Elevated temperature and CO2 stimulate late-season photosynthesis but impair cold gardening in Pine. Plant Physiol. 2016;172:802–818. doi: 10.1104/pp.16.00753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, et al. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 2003;17:1043–1054. doi: 10.1101/gad.1077503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dalmannsdottir S, Jorgensen M, Rapacz M, Ostrem L, Larsen A, Rodven R, et al. Cold acclimation in warmer extended autumns impairs freezing tolerance of perennial ryegrass (Lolium perenne) and timothy (Phleum pratense) Physiol Plant. 2017;160:266–281. doi: 10.1111/ppl.12548. [DOI] [PubMed] [Google Scholar]
  7. Ding Y, Li H, Zhang X, Xie Q, Gong Z, Yang S. OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell. 2015;32:278–289. doi: 10.1016/j.devcel.2014.12.023. [DOI] [PubMed] [Google Scholar]
  8. Ding Y, Jia Y, Shi Y, Zhang X, Song C, Gong Z, et al. OST1-mediated BTF3L phosphorylation positively regulates CBFs during plant cold responses. EMBO J. 2018;37:e98228. doi: 10.15252/embj.201798228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF. Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell. 2009;21:972–984. doi: 10.1105/tpc.108.063958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dong MA, Farre EM, Thomashow MF. Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proc Natl Acad Sci USA. 2011;108:7241–7246. doi: 10.1073/pnas.1103741108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Eremina M, Rozhon W, Poppenberger B. Hormonal control of cold stress responses in plants. Cell Mol Life Sci. 2016;73:797–810. doi: 10.1007/s00018-015-2089-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Franklin KA, Whitelam GC. Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat Genet. 2007;39:1410–1413. doi: 10.1038/ng.2007.3. [DOI] [PubMed] [Google Scholar]
  13. Gehan MA, Park S, Gilmour SJ, An C, Lee CM, Thomashow MF. Natural variation in the C-repeat binding factor cold response pathway correlates with local adaptation of Arabidopsis ecotypes. Plant J. 2015;84:682–693. doi: 10.1111/tpj.13027. [DOI] [PubMed] [Google Scholar]
  14. Guo X, Liu D, Chong K. Cold signaling in plants: insights into mechanisms and regulation. J Integr Plant Biol. 2018;60:745–756. doi: 10.1111/jipb.12706. [DOI] [PubMed] [Google Scholar]
  15. Hoermiller II, Naegele T, Augustin H, Stutz S, Weckwerth W, Heyer AG. Subcellular reprogramming of metabolism during cold acclimation in Arabidopsis thaliana. Plant Cell Environ. 2017;40:602–610. doi: 10.1111/pce.12836. [DOI] [PubMed] [Google Scholar]
  16. Jeknic Z, Pillman KA, Dhillon T, Skinner JS, Veisz O, Cuesta-Marcos A, et al. Hv-CBF2A overexpression in barley accelerates COR gene transcript accumulation and acquisition of freezing tolerance during cold acclimation. Plant Mol Biol. 2014;84:67–82. doi: 10.1007/s11103-013-0119-z. [DOI] [PubMed] [Google Scholar]
  17. Jia Y, Ding Y, Shi Y, Zhang X, Gong Z, Yang S. The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis. New Phytol. 2016;212:345–353. doi: 10.1111/nph.14088. [DOI] [PubMed] [Google Scholar]
  18. Jiang B, Shi Y, Zhang X, Xin X, Qi L, Guo H, et al. PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis. Proc Natl Acad Sci USA. 2017;114:E6695–E6702. doi: 10.1073/pnas.1706226114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kang J, Zhang H, Sun T, Shi Y, Wang J, Zhang B, et al. Natural variation of C-repeat-binding factor (CBFs) genes is a major cause of divergence in freezing tolerance among a group of Arabidopsis thaliana populations along the Yangtze River in China. New Phytol. 2013;199:1069–1080. doi: 10.1111/nph.12335. [DOI] [PubMed] [Google Scholar]
  20. Kidokoro S, Maruyama K, Nakashima K, Imura Y, Narusaka Y, Shinwari ZK, et al. The phytochrome-interacting factor PIF7 negatively regulates DREB1 expression under circadian control in Arabidopsis. Plant Physiol. 2009;151:2046–2057. doi: 10.1104/pp.109.147033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kidokoro S, Yoneda K, Takasaki H, Takahashi F, Shinozaki K, Yamaguchi-Shinozaki K. Different cold-signaling pathways function in the responses to rapid and gradual decreases in temperature. Plant Cell. 2017;29:760–774. doi: 10.1105/tpc.16.00669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kim Y, Park S, Gilmour SJ, Thomashow MF. Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J. 2013;75:364–376. doi: 10.1111/tpj.12205. [DOI] [PubMed] [Google Scholar]
  23. Kim YS, Lee M, Lee JH, Lee HJ, Park CM. The unified ICE-CBF pathway provides a transcriptional feedback control of freezing tolerance during cold acclimation in Arabidopsis. Plant Mol Biol. 2015;89:187–201. doi: 10.1007/s11103-015-0365-3. [DOI] [PubMed] [Google Scholar]
  24. Kim SH, Kim HS, Bahk S, An J, Yoo Y, Kim JY, et al. Phosphorylation of the transcriptional repressor MYB15 by mitogen-activated protein kinase 6 is required for freezing tolerance in Arabidopsis. Nucleic Acids Res. 2017;45:6613–6627. doi: 10.1093/nar/gkx417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kim YS, An C, Park S, Gilmour SJ, Wang L, Renna L, et al. CAMTA-mediated regulation of salicylic acid immunity pathway genes in Arabidopsis exposed to low temperature and pathogen infection. Plant Cell. 2017;29:2465–2477. doi: 10.1105/tpc.16.00865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Korner C. Plant adaptation to cold climates. F1000Res. 2016;5:2769–2774. doi: 10.12688/f1000research.9107.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kovi MR, Ergon A, Rognli OA. Freezing tolerance revisited-effects of variable temperatures on gene regulation in temperate grasses and legumes. Curr Opin Plant Biol. 2016;33:140–146. doi: 10.1016/j.pbi.2016.07.006. [DOI] [PubMed] [Google Scholar]
  28. Lee CM, Thomashow MF. Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2012;109:15054–15059. doi: 10.1073/pnas.1211295109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Li X, Ma D, Lu SX, Hu X, Huang R, Liang T, et al. Blue light- and low temperature-regulated COR27 and COR28 play roles in the Arabidopsis circadian clock. Plant Cell. 2016;28:2755–2769. doi: 10.1105/tpc.16.00354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Li H, Ding Y, Shi Y, Zhang X, Zhang S, Gong Z, et al. MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Dev Cell. 2017;43:630–642 e634. doi: 10.1016/j.devcel.2017.09.025. [DOI] [PubMed] [Google Scholar]
  31. Liu Y. Roles of mitogen-activated protein kinase cascades in ABA signaling. Plant Cell Rep. 2012;31:1–12. doi: 10.1007/s00299-011-1130-y. [DOI] [PubMed] [Google Scholar]
  32. Liu Y, He C. A review of redox signaling and the control of MAP kinase pathway in plants. Redox Biol. 2017;11:192–204. doi: 10.1016/j.redox.2016.12.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Liu Y, Zhou J. MAPping kinase regulation of ICE1 in freezing tolerance. Trends Plant Sci. 2018;23:91–93. doi: 10.1016/j.tplants.2017.12.002. [DOI] [PubMed] [Google Scholar]
  34. Liu Z, Jia Y, Ding Y, Shi Y, Li Z, Guo Y, et al. Plasma membrane CRPK1-mediated phosphorylation of 14-3-3 proteins induces their nuclear import to fine-tune CBF signaling during cold response. Mol Cell. 2017;66:117–128 e115. doi: 10.1016/j.molcel.2017.02.016. [DOI] [PubMed] [Google Scholar]
  35. Maurya JP, Bhalerao RP. Photoperiod- and temperature-mediated control of growth cessation and dormancy in trees: a molecular perspective. Ann Bot. 2017;120:351–360. doi: 10.1093/aob/mcx061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Menon M, Barnes WJ, Olson MS. Population genetics of freeze tolerance among natural populations of Populus balsamifera across the growing season. New Phytol. 2015;207:710–722. doi: 10.1111/nph.13381. [DOI] [PubMed] [Google Scholar]
  37. Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, et al. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell. 2007;19:1403–1414. doi: 10.1105/tpc.106.048397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Miura K, Ohta M, Nakazawa M, Ono M, Hasegawa PM. ICE1 Ser403 is necessary for protein stabilization and regulation of cold signaling and tolerance. Plant J. 2011;67:269–279. doi: 10.1111/j.1365-313X.2011.04589.x. [DOI] [PubMed] [Google Scholar]
  39. Moellering ER, Muthan B, Benning C. Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science. 2010;330:226–228. doi: 10.1126/science.1191803. [DOI] [PubMed] [Google Scholar]
  40. Nakamichi N, Kusano M, Fukushima A, Kita M, Ito S, Yamashino T, et al. Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol. 2009;50:447–462. doi: 10.1093/pcp/pcp004. [DOI] [PubMed] [Google Scholar]
  41. Newton AC, Torrance L, Holden N, Toth IK, Cooke DE, Blok V, et al. Climate change and defense against pathogens in plants. Adv Appl Microbiol. 2012;81:89–132. doi: 10.1016/B978-0-12-394382-8.00003-4. [DOI] [PubMed] [Google Scholar]
  42. Noren L, Kindgren P, Stachula P, Ruhl M, Eriksson ME, Hurry V, et al. Circadian and plastid signaling pathways are integrated to ensure correct expression of the CBF and COR genes during photoperiodic growth. Plant Physiol. 2016;171:1392–1406. doi: 10.1104/pp.16.00374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Pagter M, Arora R. Winter survival and deacclimation of perennials under warming climate: physiological perspectives. Physiol Plant. 2013;147:75–87. doi: 10.1111/j.1399-3054.2012.01650.x. [DOI] [PubMed] [Google Scholar]
  44. Park S, Lee CM, Doherty CJ, Gilmour SJ, Kim Y, Thomashow MF. Regulation of the Arabidopsis CBF regulon by a complex low-temperature regulatory network. Plant J. 2015;82:193–207. doi: 10.1111/tpj.12796. [DOI] [PubMed] [Google Scholar]
  45. Pino MT, Skinner JS, Jeknic Z, Hayes PM, Soeldner AH, Thomashow MF, et al. Ectopic AtCBF1 over-expression enhances freezing tolerance and induces cold acclimation-associated physiological modifications in potato. Plant Cell Environ. 2008;31:393–406. doi: 10.1111/j.1365-3040.2008.01776.x. [DOI] [PubMed] [Google Scholar]
  46. Puhakainen T, Li C, Boije-Malm M, Kangasjarvi J, Heino P, Palva ET. Short-day potentiation of low temperature-induced gene expression of a C-repeat-binding factor-controlled gene during cold acclimation in silver birch. Plant Physiol. 2004;136:4299–4307. doi: 10.1104/pp.104.047258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Rapacz M, Ergon A, Hoglind M, Jorgensen M, Jurczyk B, Ostrem L, et al. Overwintering of herbaceous plants in a changing climate. still more questions than answers. Plant Sci. 2014;225:34–44. doi: 10.1016/j.plantsci.2014.05.009. [DOI] [PubMed] [Google Scholar]
  48. Ruiz-Vera UM, Siebers MH, Drag DW, Ort DR, Bernacchi CJ. Canopy warming caused photosynthetic acclimation and reduced seed yield in maize grown at ambient and elevated CO2. Glob Chang Biol. 2015;21:4237–4249. doi: 10.1111/gcb.13013. [DOI] [PubMed] [Google Scholar]
  49. Shepherd TG. Effects of a warming Arctic. Science. 2016;353:989–990. doi: 10.1126/science.aag2349. [DOI] [PubMed] [Google Scholar]
  50. Shi Y, Huang J, Sun T, Wang X, Zhu C, Ai Y, et al. The precise regulation of different COR genes by individual CBF transcription factors in Arabidopsis thaliana. J Integr Plant Biol. 2017;59:118–133. doi: 10.1111/jipb.12515. [DOI] [PubMed] [Google Scholar]
  51. Shi Y, Ding Y, Yang S. Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci. 2018;23:623–637. doi: 10.1016/j.tplants.2018.04.002. [DOI] [PubMed] [Google Scholar]
  52. Soltesz A, Smedley M, Vashegyi I, Galiba G, Harwood W, Vagujfalvi A. Transgenic barley lines prove the involvement of TaCBF14 and TaCBF15 in the cold acclimation process and in frost tolerance. J Exp Bot. 2013;64:1849–1862. doi: 10.1093/jxb/ert050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Thomashow MF. PLANT COLD ACCLIMATION: Freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol. 1999;50:571–599. doi: 10.1146/annurev.arplant.50.1.571. [DOI] [PubMed] [Google Scholar]
  54. Tondelli A, Francia E, Barabaschi D, Pasquariello M, Pecchioni N. Inside the CBF locus in Poaceae. Plant Sci. 2011;180:39–45. doi: 10.1016/j.plantsci.2010.08.012. [DOI] [PubMed] [Google Scholar]
  55. Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J. 2005;41:195–211. doi: 10.1111/j.1365-313X.2004.02288.x. [DOI] [PubMed] [Google Scholar]
  56. Wang P, Cui X, Zhao C, Shi L, Zhang G, Sun F, et al. COR27 and COR28 encode nighttime repressors integrating Arabidopsis circadian clock and cold response. J Integr Plant Biol. 2017;59:78–85. doi: 10.1111/jipb.12512. [DOI] [PubMed] [Google Scholar]
  57. Welling A, Palva ET. Involvement of CBF transcription factors in winter hardiness in birch. Plant Physiol. 2008;147:1199–1211. doi: 10.1104/pp.108.117812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Wisniewski M, Norelli J, Bassett C, Artlip T, Macarisin D. Ectopic expression of a novel peach (Prunus persica) CBF transcription factor in apple (Malus × domestica) results in short-day induced dormancy and increased cold hardiness. Planta. 2011;233:971–983. doi: 10.1007/s00425-011-1358-3. [DOI] [PubMed] [Google Scholar]
  59. Yang T, Chaudhuri S, Yang L, Du L, Poovaiah BW. A calcium/calmodulin-regulated member of the receptor-like kinase family confers cold tolerance in plants. J Biol Chem. 2010;285:7119–7126. doi: 10.1074/jbc.M109.035659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Zhao C, Zhang Z, Xie S, Si T, Li Y, Zhu JK. Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiol. 2016;171:2744–2759. doi: 10.1104/pp.16.00533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Zhao C, Wang P, Si T, Hsu CC, Wang L, Zayed O, et al. MAP kinase cascades regulate the cold response by modulating ICE1 protein stability. Dev Cell. 2017;43:618–629 e615. doi: 10.1016/j.devcel.2017.09.024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Zhen Y, Ungerer MC. Relaxed selection on the CBF/DREB1 regulatory genes and reduced freezing tolerance in the southern range of Arabidopsis thaliana. Mol Biol Evol. 2008;25:2547–2555. doi: 10.1093/molbev/msn196. [DOI] [PubMed] [Google Scholar]

Articles from Plant Cell Reports are provided here courtesy of Springer

RESOURCES