ASAgricultural Sciences2156-8553Scientific Research Publishing10.4236/as.2023.142017AS-123315ArticlesBiomedical&Life Sciences Earth&Environmental Sciences Low-Temperature Signaling Pathways and Their Signaling Factors in Plant JianpingLi1*ZhiqingLiu2XiaoyanHao3XiaochunChang1ZhunZhao1GuoChen1WenranHu1ShengqiGao1QuanshengHuang1Xinjiang Key Laboratory of Crop Biotechnology, Urumqi, ChinaInstitute of Economic Crops, Xinjiang Academy of Agricultural Sciences, Urumqi, ChinaInstitute of Nuclear Technology and Biotechnology, Xinjiang Academy of Agricultural Sciences, Urumqi, China15022023140225626818, January 202324, February 2023 27, February 2023© Copyright 2014 by authors and Scientific Research Publishing Inc. 2014This work is licensed under the Creative Commons Attribution International License (CC BY). http://creativecommons.org/licenses/by/4.0/

Low temperature as abiotic stress adversely impacts plant growth and development, and limits the ecological distribution of plants as well. Throughout their long evolutionary history, plants have developed a range of complicated and precise molecular regulatory mechanisms to deal with low-temperature stress, involving the activation of signal transduction pathways and the regulation of related genes. In this review, we provide a systematic summary of the most recent research findings regarding three hypotheses of cellular perception of low-temperature signals and two major intracellular low-temperature signaling pathways, including CBF-dependent signaling pathways and CBF-independent signaling pathways. Focus is placed on the functions of each component of the ICE-CBF-COR signaling cascade as well as their interrelationships. This review concludes that although some progress has been made in the identification, function, and mechanism of low-temperature response genes, their roles in the low-temperature regulatory network and molecular mechanisms still need to be studied in detail, which will be of great significance for improving the low-temperature tolerance of plants and adapting to climate change.

Low Temperature Signaling CBF COR Signaling Factors1. Introduction

Temperature, as one of the important environmental factors, always accompanies the whole life cycle of plants, influencing their growth and development and limiting their ecological distribution. Low temperature can negatively affect plant growth and development, which is one of the abiotic stresses, called low-temperature stress. Throughout their long evolutionary history, plants have developed a variety of physiological and molecular mechanisms to adapt to the low-temperature environment and increase their tolerance to low temperatures [1] . With the advent of molecular biology, it has been found that low-temperature stress signal from perception involves different regulatory networks, which are complex and refined. Significant progress has been made in understanding the regulatory networks involved in cold tolerance over the past ten years. In many plants, a large number of transcription factors have been found that mediate cold signaling and regulate the expression of cold regulons [2] . It is composed of many proteins known as Cold-Regulated (COR) proteins and the essential transcriptional factors ICE (Inducer of CBF Expression) and CBF (C-repeat-Binding Factor). Other activators or repressors, in addition to the fundamental components of the ICE, CBF, and COR genes, are engaged in this pathway, and either directly or indirectly, contribute to cold tolerance [3] . Additionally, it has been demonstrated that plant hormones, the circadian clock, and light play significant roles in the response to cold stress. Although the ICE-CBF-COR pathway is the best-studied and important for plants’ ability to tolerate low temperatures and homologous genes from this pathway have been identified in a diversity of cold-tolerant and sensitive plants, there are still many questions regarding the regulation and function of these genes, our knowledge of the regulation network involving CBF genes is still insufficient.

In this paper, we review the most recent research findings on low-temperature signaling pathways in recent years, focusing on the functions and interrelationships of each component of the low-temperature ICE-CBF-COR signaling cascade.

2. Plant Perception of low-Temperature Signals

When plants are exposed to low temperatures, they must first detect the signal for low temperatures. It is unclear, however, how plants perceive the low-temperature signal and transmit it to the nucleus to activate transcription factors that regulate gene expression and initiate a series of physiological and biochemical responses. There is no direct evidence to support the notion that membrane-based proteins serve as signal receptors for the perception of low-temperature signals, and few new forms of signal receptors have been described. Three hypotheses exist about the perception of low-temperature stress signals: 1) Ca2+ channel hypothesis, which proposes that temperature changes affect cell membrane fluidity, which in turn affects the structure and/or activity of membrane-localized proteins such as Ca2+ channels, resulting in changes in Ca2+ concentration on both sides of the cell membrane and generating calcium ion flow, a process that induces the expression of temperature-responsive genes [4] . It was found that the G-protein regulators COLD1 (Chilling-Tolerance Divergence 1) and RGA1 (Rice G-protein Alpha subunit 1) in rice can control the perception of low-temperature signals and extracellular calcium ion influx in a synergistic manner [5] . OsCIPK7 (Oryza sativa Calcineurin B-like interacting protein kinases 7) detects low-temperature signals by adjusting its protein structure in response to variations in calcium ion concentration [6] . By controlling calcium ion concentration, CNGCs (Cyclic Nucleotide-Gated Ca2+ Channels), a crucial regulator of plant growth and development and stress response, can increase the cold tolerance of Arabidopsis and Moss [7] [8] . However, it is unclear how COLD1 or CNGCs regulate calcium ion influx during low-temperature stress. Therefore, determining which Ca2+ channels are involved in the perception of low-temperature signals remains to be deeply explored. The prevailing view is that Ca2+ acts as a second messenger mediating the transmission of cryogenic signals from extracellular to intracellular via calcium-binding proteins such as Calmodulin (CaM), Calcium-Dependent Protein Kinase (CDPK), CBL-Interacting Protein Kinase (CIPK) and proteins of the B subunit of Calcineurin-B Like (CBL) protein. It has been shown that CDPKs antagonist (W7) suppresses low-temperature response gene expression in alfalfa and Arabidopsis [9] [10] ; while low-temperature stress significantly increases autophosphorylation and kinase activity of rice CIPK7, suggesting that low-temperature stress is involved in post-translational regulation of CIPK [6] . Similarly, Arabidopsis CBL and CIPK proteins were found to participate in low-temperature signaling in a Ca2+-dependent manner [11] . These primary groups of calcium-binding proteins bind calcium ions and undergo conformational changes to effectively regulate the expression of target genes. 2) MAPKs hypothesis, Mitogen-Activated Protein Kinases (MAPKs) are a class of intracellular serine/threonine protein kinases with diverse signaling functions in eukaryotic cells. A typical MAPK module consists of three protein kinases: MAPase Kinase Kinase (MKKK or MEKK), MAPase Kinase (MKK or MEK), and MAP Kinase (MAPK or MPK), which are mutually activated by cascade reactions phosphorylation to transmit signals of adversity stress including low temperature, high salt, and drought [12] . In plants, many MAPK family members respond to low-temperature stress such as the kinase activity of alfalfa MMK4 is increased under low temperature stress [13] ; the expression of Arabidopsis MPK3, MPK4 and MPK6 genes can reach very high levels within a very short time after low-temperature stress [14] . In Arabidopsis, under low-temperature induction, CRLK1 activates MEKK1, which in turn activates MPK4 by phosphorylating MKK2 to form the MEKK1-MKK2-MPK4 cascade signaling pathway, and the activation of the MEKK1-MKK2-MPK4 signaling pathway inhibits the activation of the MKK4/5-MPK3/6 cascade signaling pathway, resulting in enhanced low-temperature tolerance in Arabidopsis [15] . 3) Phosphatase hypothesis, despite the limited number of phosphatases identified to date that can detect low-temperature signals, members of this group play crucial roles in the low-temperature signal transduction pathway. It was found that Arabidopsis histidine kinase AtHK1 is up-regulated by low-temperature induction and transmits low-temperature stress signals to the nucleus through phosphorylation [16] ; Bacillus subtilis histidine kinase K acts as a temperature receptor to regulate the expression of desaturase [17] ; Phosphoprotein phosphatase PP2A and PP2B regulate low-temperature signaling by activating or inactivating MAP kinases and CDPKs [18] ; Arabidopsis CRLK1, a Ca2+/CaM receptor kinase, enhances low-temperature tolerance in Arabidopsis by positively regulating COR gene expression through phosphorylation of MEKK1 [19] .

3. Low-Temperature Signaling Pathways

It is a complicated signaling process from receiving the low-temperature signal to producing the corresponding response, which generates a multi-branched signaling regulatory network in the cell. Numerous studies have demonstrated the involvement of the transcription factors CBF (C-repeat Binding Factor) as a significant regulatory factor. Based on the roles of CBFs in the regulation network of low-temperature signaling, the intracellular transduction of signals has been divided into two pathways: CBF-dependent and CBF-independent pathways.

3.1. The CBF-Dependent Signaling Pathway

Among the CBF-dependent signaling pathways, the ICE-CBF-COR signaling pathway is one of the most thoroughly investigated CBF-dependent pathways. ICE (Inducer of CBF Expression), CBF, and many Cold-Regulated (COR) proteins are its core components, of which the most critical component is CBF. Besides ICE, CBF, and COR, many related activators and repressors are as well engaged in this pathway and play crucial roles in the cold response [20] . Arabidopsis contains four members of the CBF gene family: CBF1/DREB1B, CBF2/DREB1C, CBF3/DREB1A, and CBF4. CBF1-CBF3 expression is induced by low temperature. Regardless CBF4 expression is not induced by low temperature, overexpression of CBF4 improves plant cold and drought resistance [21] . The CBF single, double, and triple mutants all exhibit a low-temperature sensitive phenotype, with the cbf123 triple mutant being the most sensitive to low temperature [22] . Upon low-temperature stimulation, CBF1-CBF3 stimulates COR gene expression by binding directly to the CRT/DRE cis-acting region of the COR promoters [23] . Overexpression of CBF1 upregulates COR expression, as indicated by an increase in cold tolerance in Arabidopsis [24] . Recently, it was also found that low-temperature-induced CBF interacts with PIF3 to enhance the stability of PHYB, which in turn enhances the low-temperature tolerance of Arabidopsis [25] . CBF homologs in rice, tomato, wheat, barley, and maize have been identified and demonstrated that their transcripts are induced by low temperature [26] , and PtCBF1, PtCBF2, PtCBF3, and PtCBF4 gene expression levels are upregulated in poplar leaves under low-temperature conditions [27] .

The ICE gene family was discovered later than the CBF family, and in 2003, Chinnusamy et al. found that ICE1 activates CBF gene expression by binding directly to the promoter of the CBF gene. The ice1 mutant exhibits reduced tolerance with suppressed expression of the CBF gene at low temperatures [28] . ICE2 was found to similarly function as a positive regulator of CBF with low-temperature induction [29] . ICE homologs including CbICE53 in caper [30] , CsICE1 in tea [31] , CdICE1 in chrysanthemum [32] , SlICE1 in tomato [33] , VaICE1 and VaICE2 in grape [34] , RsCIE1 in radish [35] and ZmICE1 in maize [36] were found to be responsive to low-temperature stress. In Arabidopsis, Overexpression of wheat TaICE41 and TaICE87, which are highly homologous to Arabidopsis ICE1, stimulated the expression of AtCBF2 and AtCBF3 and enhanced Arabidopsis’ tolerance to low temperatures [37] . Meanwhile, recent studies indicate that the MAPK signaling pathway modulates the transcription of CBFs via regulating the expression of ICE1, thus supporting the possibility of multiple regulatory networks upstream of CBF [38] .

In the early 1990s, a group of genes, namely COR genes, were found to play key roles in plant response to low-temperature stress [39] , and further studies revealed that the ability of plants to tolerate low temperatures was largely dependent on the regulation of COR gene expression [40] . It is notable that the term “COR genes” broadly refers to all genes that are responsive to cold, including the cold-regulated gene COR, the low-temperature-inducible gene LTI, and the cold-inducible gene KIN [41] . The expression products of these “COR genes” are various types of proteins or biomolecules, including enzymes, molecular chaperones, and antifreeze proteins related to plant respiration, glucose metabolism, lipid metabolism, etc. Certain of these proteins and biomolecules restore cell metabolism at low temperatures, maintain cell membrane stability, and act directly as antifreeze proteins to protect cells from low-temperature injury [23] . COR genes in the narrow concept refer to cold regulated genes, which share the common feature of containing a CRT/DRE cis-acting element in the promoter that can bind directly to CBF genes. The COR genes described in this review are genes in the narrow sense of the concept. The expression of COR components, which are located downstream of the ICE1-CBF-COR pathway are crucial for low-temperature defense [40] . Studied have demonstrated that the COR47 [42] , COR78 [43] , COR6.6 [44] , and COR15a [45] genes act as positive regulators in Arabidopsis, and Arabidopsis COR27 and COR28 negatively regulate the plant’s response to cold temperatures [46] . Expression of COR homologs from other species such as BN28 (BnaAnng37980D, Kin1) and BN115(COR15) in oilseed rape [47] , COR14b in barley, WCOR410 and WCOR14 in wheat, CsCOR1 in tea, BpCOR25 gene in Chinese cabbage [48] and COR27 in cotton [49] are all mediated by low-temperature induction. Furthermore, COR genes are also involved in other aspects of plant development and growth. Arabidopsis COR27 and COR28 induced by blue light and low temperature positively control flowering time and biological rhythm [46] , and interact with light signaling factors COP1 (Constitutively Photomorphogenic 1) SPA1 (Suppressor of PHYA-105) or HY5 (Elongated Hypocotyls 5) to inhibit photomorphogenesis promoting hypocotyl elongation in response to light [50] . Thus, it was suggested that COR genes not only act in the low-temperature signaling pathway but also in other signaling pathways.

Likewise, CRT (C-Repeat)/DRE (Dehydration Response Element) elements both containing CCGAC core sequences are of interest as important low-temperature response components, which were found as dehydration response elements by Shinozaki and Baker in 1994 [41] . CRT/DRE elements identified from the promoters of COR members of Arabidopsis KIN1, COR6.6 [44] , and RD29A (Responsive to Dehydration 29 of Arabidopsis) [51] , oilseed rape BN115 [52] , wheat WCS120 [53] were found to respond to abiotic stresses such as low temperature, drought, and salt. It was also discovered that the Arabidopsis RD29A promoter regulates the AtSOC1 (Arabidopsis Suppressor of Cytokine signaling 1) gene to promote early flowering in Chrysanthemum upon induction of drought stress [54] .

Interestingly, the CBF signaling pathway is also modulated by post-transcriptional regulation of genes, including pre-mRNA processing, translocation, and translation. Pre-mRNA splicing is an essential process for gene function. For instance, low-temperature induced STA1 (Stabilized 1) protein selectively splice the COR gene intron thereby regulating COR gene expression [55] . NUPs (Nucleoporins) proteins mediate the translocation of RNAs and proteins between the nucleus and cytoplasm and alter the accumulation of CBF and other low-temperature-responsive mRNAs in the nucleus in response to low-temperature stimulation [56] . Arabidopsis HOS1 (High expression of Osmotically responsive gene 1) gene promotes the ubiquitinated degradation of phosphorylated ICE1 by binding with phosphorylated ICE1, consequently repressing the transcription of CBF and its downstream genes [57] . Kinases such as MAPKs, CDPKs, and RLKs (Receptor-Like Kinases) exert regulatory functions on the CBF signaling pathway through phosphorylation [58] .

3.2. The CBF-Independent Signaling Pathway

Not all COR genes are directly regulated by CBF proteins. Analysis of the Arabidopsis transcriptome revealed that only 12% of COR genes are regulated by CBF [59] . Studies on the promoters of COR genes activated by CBF in Arabidopsis showed that approximately 38% of genes do not have a CRT in a region 1000 bp upstream of the ATG start codon [60] . Despite the involvement of HSFC1 (Heat Shock Factor 1), ZAT12 (Zinc finger of Arabidopisis Thaliana 12), and CZF1 (Phytophthora infestans CFZ1-like protein) in regulating COR gene expression, their expression in the cbf123 triple mutant was not affected, indicating that the regulation of COR genes by HSFC1, ZAT12, and CZF1 is not dependent on CBF but is functional in low-temperature signaling [3] . Further, CBF expression was not altered in Arabidopsis esk1 (Eskimo 1) mutants, but the mutants showed a constitutive cold-tolerant phenotype [61] ; Gigantea (GI), a group of proteins controlling nuclear localization, participated in the modulation of flowering and circadian rhythms in a cold-induced manner independent of the CBF pathway, and gi-3 mutants showed a reduced capability for cold tolerance [62] .

Plant hormones exhibit regulatory effects on signaling and downstream gene expression during the low-temperature stress. JAZs (Jasmonate ZIM-domains) interact with EIN3/EIL1 (Ethylene-Insensitive 3/Ethylene-Insensitive 3-Like 1) to mediate JA (Jasmonic Acid), ETH (Ethylene), and CBF signaling, whereas the competitive binding of DELLA (RGA-like protein) to PIF4-BRZ1 (Phytochrome-Interacting Factor 4-Brassinzaole Resistant 1) modulates the GA (Gibberellin Acid), BR (Brassinosteroid), and CBF signaling pathways [11] . Among the CBF-independent low-temperature regulatory mechanisms, ABA (Abscisic Acid)-dependent signaling transduction pathways have been investigated for many years, and studies of the Arabidopsis transcriptome indicated that 10% of ABA-responsive genes also respond to low-temperature stress [63] . Some COR genes, such as RD29A, RD22, COR15A, and COR47, contain ABA-responsive (ABRE) cis-elements activated by ABRE-binding proteins/factors (AREBs/ABFs) in addition to CRT/DRE-acting elements in their promoters [64] . Numerous regulatory factors in ABA biosynthesis and signaling pathways play crucial roles in COR gene expression, according to genetic research [62] . ABI3 (ABA Insensitive 3) as an ABRE-binding protein overexpressed in Arabidopsis resulted in enhanced COR gene expression in asexual tissues [65] . PHYA (Phytochrome A) and PHYB (Phytochrome B) negatively regulate the low-temperature response in Arabidopsis in an ABA-dependent manner [66] .

4. Conclusion and Future Perspectives

Even though remarkable progress has been made in recent years in elucidating the molecular mechanisms of plant responses to low-temperature stress, the question of how plants perceive low-temperature signals has not yet been fully answered, and the various hypotheses proposed need to be supported by more evidence. Upon low-temperature perception, plants activate different types of complicated low-temperature signaling pathways in a CBF-dependent and CBF-independent manner, and despite the fact that CBF-dependent signaling pathways have been well explored, a number of crucial issues remain to be investigated. Many CBF-regulated low-temperature response genes, for instance, are functional in enhancing low-temperature tolerance in plants, but further studies are required to identify which of these genes play a crucial role and how they function. In addition, more signaling factors have been identified in both CBF-mediated and non-CBF-mediated signaling pathways, and these newly identified signaling factors play key or essential roles in other aspects of plant growth and development besides responding to low-temperature stress such as Arabidopsis COR27 and COR28 genes were found to be involved in the regulation of low-temperature response, photomorphogenesis, flowering time, and biological rhythms [49] [50] . The photoreceptors PHYA and PHYB, as well as COP1, SPA1, and HY5, which are major signaling components in the light signaling pathway, have been successively identified as being involved in the low-temperature response [50] [66] . The key roles of plant hormones in the low-temperature response have been proven, but the crosstalks between low-temperature signaling and phytohormones signaling, which are necessary for activating downstream genes essential for plant development and response to low temperature, and potential mechanisms of hormone signaling in the regulation of the low-temperature response still require investigation. We believe it will be the focus of ongoing studies, triggering the consideration of whether there is a balance between the regulatory network of plant development and the regulatory network of adversity to stabilize the whole regulatory network. In conclusion, even though there are still many remaining questions regarding how plants respond to low-temperature stress, these will be eventually addressed with continuous exploration.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant nos.32260449) and the Science and Technology Innovation Base Construction Program of Xinjiang Uygur Autonomous Region—Resource Sharing Platform Construction (Grant nos.PT2222).

Conflicts of Interest

The authors declare no conflicts of interest regarding the publication of this paper.

Cite this paper

Li, J.P., Liu, Z.Q., Hao, X.Y., Chang, X.C., Zhao, Z., Chen, G., Hu, W.R., Gao, S.Q. and Huang, Q.S. (2023) Low-Temperature Signaling Pathways and Their Signaling Factors in Plant. Agricultural Sciences, 14, 256-268. https://doi.org/10.4236/as.2023.142017

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