Low temperature is one of the abiotic stress factors that limits plant growth and development, and geographical distribution. According to the damage degree of low temperature to plants, it can be divided into chilling stress (0℃~15℃) and freezing stress (<0°C). Chilling stress mainly limits the growth and development of plants by inducing cell membrane stiffness, damaging protein structure and function, and inhibiting plant antioxidant activity and photosynthesis (Orvar et al., 2000; Siddiqui and Cavicchioli, 2006). In contrast, freezing stress caused more serious damage to plants, which caused physical damage to cell membrane by inducing the formation of ice nuclei in the cytoplasm, and eventually led to severe dehydration and even death of cells (Pearce, 2001). In tropical and subtropical regions, chilling stress is the main form of low temperature stress, which affects the yield and quality of important economic crops such as rice (Oryza sativa), soybean (Glycine max), maize (Zea mays) and tomato (Solanum lycopersicum) (Chinnusamy et al., 2007). However, in temperate regions, chilling stress can induce plants to produce low-temperature acclimation mechanism, thereby improving the freezing resistance of plants (Chinnusamy et al., 2007). The freezing resistance of plants directly depends on their ability to inhibit the formation of intracellular ice crystals. When plants are exposed to unfrozen low temperatures, they acquire higher cold tolerance, known as cold acclimation (Chinnusamy et al., 2007).

Cold acclimation is one of the main strategies for plants to adapt to cold stress. In the process of cold acclimation, plants mainly synthesize osmotic adjustment substances (such as soluble sugar and proline) and low temperature protective proteins (such as late embryogenesis abundant protein, antifreeze protein and cold shock protein) to enhance the ability of plants to resistant low temperature (Thomashow, 1999; Kaplan et al., 2007). In the past two decades, researchers have identified many core components and components including messengers, protein kinases, phosphatases, and transcription factors from low temperature response signaling pathways based on cold acclimation. Among them, CBF-COR signal pathway has the most complete description. In this pathway, CBF/DREB1 (C-repeat binding factor/dehydration-responsive element-binding protein 1) gene was rapidly induced by low temperature and played a key role in plant cold acclimation (Stockinger et al., 1997; Liu et al., 1998), while CORs mainly encoded osmotic adjustment substance synthase and low temperature protective protein, including a series of functional genes such as COR, LTI and KIN (Yamaguchi-Shinozaki and Shinozaki, 1994; Shi et al., 2018). CBFs protein directly binds to the CORs promoter and induces its expression, thereby improving the cold tolerance of plants (Stockinger et al., 1997; Liu et al., 1998). Understanding the molecular regulation mechanism of plant response to cold stress can provide valuable genetic information and gene resources for improving genetic improvement of plant tolerance to low temperature and molecular breeding tolerance. This study systematically reviews the latest molecular regulatory networks and mechanisms of plant response to cold stress in recent years and discusses the future research directions and priorities in this field.

1 CBF-COR Pathway

When plants are exposed to non-frozen cold stress, CBFs gene can be rapidly induced and up-regulated within 15 min, and then activate the downstream CORs, which is called CBF-COR regulator. There are four CBFs genes (CBF1~4) in Arabidopsis genome, which are arranged in tandem on chromosome 4. Except for CBF4, cold stress can induce CBF1~3 to bind to CRT/DRE cis-acting elements of CORs promoter, thereby activating the expression of CORs (Stockinger et al., 1997; Gilmour et al., 1998; Liu et al., 1998) (Table 1). Heterologous expression of Arabidopsis thaliana CBFs in different species can improve the freezing resistance of plants, and heterologous expression of CBFs in different species of Arabidopsis thaliana can also improve the freezing resistance of plants (Gilmour et al., 2000; Zhang et al., 2004; Savitch et al., 2005), indicating that the function of CBFs is relatively conservative in species with or without cold acclimation (Mizoi et al., 2012). The studies on single mutant, double mutant and tertiary mutant of CBF1-3 in Arabidopsis showed that cbf1/cbf2/cbf3 were most sensitive to freezing stress (Jia et al., 2016; Zhao et al., 2016). Further transcriptome analysis showed that about 10%~20% of CORs expression was dependent on CBF pathway, and there were a large number of overlapping genes in three mutants (Jia et al., 2016; Zhao et al., 2016), indicating that CBFs played a key regulatory role in plant cold tolerance, but the function was redundant. At present, homologous genes of CBFs have been identified in crops including Oryza sativa, Lycopersicon esculentum, Zea mays, Triticum aestivum and Hordeum vulgare (Shi et al., 2018), most of which are induced by cold stress and have the function of plant tolerance to cold stress (Table 1).

Table 1 Homologous genes of CBFs and their functions in known reported species

2 CBF Transcription Regulation

CBF signaling pathway integrates many internal development and external environmental signals, and is positively and negatively regulated by factors such as low temperature, circadian rhythm, photoperiod, flowering and hormones.

2.1 ICE transcription factor regulation

So far, the most clearly studied CBFs transcription activator is MYC bHLH transcription factor ICE1 (Inducer of CBF expression 1) (Chinnusamy et al., 2003). Arabidopsis ICE1 is constitutively expressed in leaves, stems and other tissues, and its encoded protein up-regulates the expression of CBFs under cold stress by binding to the MYC site (CANNTG) in the CBF1-3 promoter (Chinnusamy et al., 2003; Kim et al., 2015a). The ice1 mutant showed decreased expression abundance and freezing resistance of CBF1-3, while the ICE1 overexpression line enhanced the expression of CBF1-3 and freezing resistance of plants (Chinnusamy et al., 2003; Ding et al., 2015). In rice, the homologous protein bHLH002 of ICE1 is also involved in the regulation of cold tolerance. Both osbhlh001 knockout mutants and RNAi lines showed cold sensitivity, while overexpression of OsbHLH002 significantly improved plant cold resistance (Zhang et al., 2017). In addition, ICE2 is a paralogous protein of ICE1, which regulates CBF1 expression in function (Fursova et al., 2009; Kim et al., 2015a). Interestingly, ICE1/2 is specifically expressed in leaf stomatal cells (Kanaoka et al., 2008; Fursova et al., 2009). Previous studies have shown that low temperature reduces stomatal aperture by inducing guard cells of Commelina communis to uptake extracellular calcium (Wilkinson et al., 2001). However, it is not clear whether CBF signaling pathway is involved in regulating stomatal development and movement during cold acclimation.

2.2 Ca²⁺ signaling regulation

Early studies have shown that the CAMs (Ca²⁺-responsive protein calmodulins) are essential for the CORs expression (Polisensky and Braam, 1996). Recent studies have found that CAMTAs (Calmodulin-binding transcription activators) have conserved CAM binding sites, which can positively regulate freezing resistance of Arabidopsis by activating the expression of CBFs (Figure 1). However, different CAMTAs members specifically activate different CBFs (Doherty et al., 2009; Kim et al., 2013). In which, CAMTA1-5 positively regulates the expression of CBF1 and CBF2 (Kidokoro et al., 2017), and CAMTA3 and CAMTA5 regulate the expression of CBF1 in response to rapidly decreasing temperatures (Kidokoro et al., 2017). These results confirmed the role of CAMTAs protein in cold acclimation, indicating that CAMTAs were the hub connecting Ca²⁺ and CBFs expression. However, how the cold signal activates CAMTAs and which components are the auxiliary factors of CAMTAs remain to be further studied.

2.3 Regulation of MYB transcription factors and photosensitive pigments

MYB15 is a member of the R2R3 MYB transcription factor family. Arabidopsis thaliana MYB15 was up-regulated by low temperature, and MYB15 protein was bound to CBFs promoter element after interacting with ICE1 to regulate plant freezing resistance. Overexpression of MYB15 resulted in the decrease of CBFs expression and plant freezing resistance, while myb15 mutant showed increased CBFs expression and plant freezing resistance, indicating that MYB15 negatively regulated CBFs expression (Agarwal et al., 2006). Recent studies have shown that Arabidopsis MPK6 phosphorylates MYB15 at Ser168 site to reduce the binding affinity of MYB15 to CBF3 promoter, thereby releasing the inhibition of CBF3 gene expression by MYB15 and improving plant freezing resistance (Kim et al., 2017) (Figure 1), indicating that MPK6-mediated regulation of MYB15 plays an important role in signal transduction of cold stress in Arabidopsis. Unlike Arabidopsis, rice OsMYB3R-2 upregulates cyclin gene OsCycB1;1 and OsDREB1s expression confer plant cold tolerance (Ma et al., 2009), while OsMYBS3 negatively regulates plant cold tolerance by inhibiting OsDREB1B expression (Su et al., 2010), indicating that different MYBs in different species or in the same species have different regulatory roles in cold stress response. Environmental temperature regulates many aspects of plant growth and development, but its sensors are still unclear. It has been reported that the temperature sensitivity of PhyB (Phytochrome) is regulated by ambient temperature. PhyB participates in temperature sensing and regulation of key target genes by transforming from active Pfr state to inactive Pr state (Legris et al., 2016). bHLH transcription factors PIFs (Phytochrome-interacting factors), as the interacting proteins of PhyB, play a central role in the regulation of optical signal network (Leivar et al., 2008). Recent studies have found that PIF3 down-regulates its expression by directly binding to the CBFs promoter, thus acting as a negative regulator of freezing resistance in Arabidopsis. Under dark and cold situation, PIF3 inhibits the transcription of CBFs by directly binding to G-box and E-box of CBFs promoter, thereby negatively regulating freezing resistance of Arabidopsis (Jiang et al., 2017) (Figure 1). These results showed that negative regulatory transcription factors played an important role in maintaining the homeostasis of CBFs transcriptional regulatory network during cold acclimation.

Figure 1 Molecular regulatory network of plant response to low temperature Note: The black line: Regulated pathway of Arabidopsis under low temperature; The red line: Regulated pathway of rice under low temperature

2.4 Circadian clock and flowering regulation

Early studies found that the expression of CBFs was regulated by the circadian clock (Fowler et al., 2005). After that, Dong et al. (2011) found that the CCA1 (Circadian clock-associated 1) and LHY (Late elongated hypocotyl) positively regulated CBFs expression and plant freezing resistance. In the double mutant cca1-11/lhy-21, the expression of CBFs and plant freezing resistance were significantly decreased, indicating that CCA1/LHY-mediated circadian rhythm output could endow Arabidopsis with freezing resistance by regulating CBF cold response pathway. CCA1 has two variable shear bodies, CCA1α and CCA1β. After interaction, the special base sequence of CCA1α can be inhibited to bind to enzymes or special transcription factors, but this process can be reversed by low temperature (Seo et al., 2012). The difference is that other clock elements. Like PRRs (Pseudo-response regulators), negatively regulate CBFs expression and plant freezing resistance (Nakamichi et al., 2009). SOC1 (Suppressor of overexpression of constans 1) and FVE mediate the direct relationship between cold signal and flowering time (Boss et al., 2004). SOC1 is a kind of MADS-box transcription factor that negatively regulates the expression of CBFs by directly binding to the CArG box element in the promoter of CBFs (Seo et al., 2009), while FVE is a homologous protein in Arabidopsis related to retinoblastoma and is also involved in the negative regulation of CBF pathway (Kim et al., 2004).

2.5 Hormone regulation

Hormone signaling elements are also involved in CBFs regulation. EIN3 (Ethylene insensitive 3) is a key transcription factor in ethylene signaling. EIN3 negatively regulates the freezing tolerance of Arabidopsis thaliana by binding to the EBS motif in CBFs promoter (Shi et al., 2012). However, the EBF1/2 (EIN3-BINDING F-BOX, EBF) can ubiquitously degrade the two negative regulatory factors EIN3 and PIF3, thus positively regulating the expression of CBFs (Shi et al., 2012; Jiang et al., 2017) (Figure 1). Low temperature can induce lipogenic plant hormone jasmonic acid to relieve the inhibition of JAZ1/4 (jasmonic acid signaling pathway inhibitor ZIM-domain protein) on ICE1/2, and positively regulate the transcription of ICE and the expression of CBF1-3 (Hu et al., 2013) (Figure 1). Recently, the function of brassinosteroids in regulating freezing tolerance in Arabidopsis has also been confirmed. Mutations of BIN2 (Brassinosteroid-insensitive 2) and its homologous genes can enhance freezing resistance of plants (Li et al., 2017b). On the contrary, the three transcription factors BZR1 (Brassinazole-resistant 1), BES1 (BIN1-EMS-Supressor 1) and CESTA (CES) downstream of BIN2 positively regulate the expression of CBFs and plant freezing resistance (Eremina et al., 2017; Li et al., 2017b) (Figure 1). In rice, OsMYB30 interacts with OsJAZ9 to inhibit β-amylase gene expression and cold tolerance (Lv et al., 2017). Recent studies have found that the HAN1 gene encoding oxidase ('HAN' means 'cold' in Chinese) can catalyze the transformation of jasmonic acid into inactive jasmonic acid, and mediate JA-regulated cold tolerance at seedling stage in japonica rice (Mao et al., 2019). Besides, population genetics and association studies have confirmed that OsbZIP73, a positive regulator of cold tolerance in rice seedling stage, regulates the levels of reactive oxygen species and abscisic acid in plants by interacting with OsbZIP71 to improve cold tolerance (Liu et al., 2018). LTG1 (Low temperature growth 1) encodes a casein kinase that regulates rice growth at low temperatures through auxin-dependent pathways (Lu et al., 2014). These findings suggest that plants can better adapt to cold stress by integrating hormones and cold signaling pathways, and the interaction between hormones and cold signals will provide new insights into how plants accurately coordinate and balance growth and development and cold tolerance.

3 Post Translation Regulation of Cold Signaling Pathway

In summary, transcription factor ICE1 can activate the expression of CBF-CORs (Chinnusamy et al., 2003; Lee et al., 2005). However, the expression of ICE1 itself was not affected by low temperature (Miura et al., 2007), indicating that post translation modification of proteins affected the function of ICE1. In fact, multiple processes including protein phosphorylation, ubiquitination and SUMOylation can synergistically or antagonistically regulate the stability and abundance of ICE1 under cold stress, thereby controlling the transition and homeostasis of ICE1 protein under cold stress.

3.1 Phosphorylation regulation

Low temperature induced a sharp increase in intracellular Ca²⁺ concentration. CRLK1 and CRLK2 (calcium/calmodulin-regulated receptor-like kinases, CRLK) positively regulate the freezing resistance of Arabidopsis thaliana by inhibiting the activity of protein kinase MPK3/6 (Yang et al., 2010; Zhao et al., 2017), indicating that CRLK is the key link between calcium/calmodulin signal and low temperature signal (Figure 1). Arabidopsis MPK3/6 is a negative regulator of CBF signaling pathway (Li et al., 2017a; Zhao et al., 2017). Low temperature reduces the stability of ICE1 and the binding activity of CBF3 promoter by activating the interaction between MAPK3/6 and ICE1 and making it phosphorylated, which eventually leads to the decrease of plant freezing resistance (Li et al., 2017a; Zhao et al., 2017) (Figure 1). Different from Arabidopsis thaliana, rice OsMAPK3 phosphorylates OsbHLH002/OsICE1 to prevent RING E3 linker OsHOS1-mediated ubiquitination degradation, thereby enhancing OsICE1 protein stability and up-regulating OsTPP1 (Trehalose-6-phosphate phosphatase 1) gene, which ultimately confers strong cold tolerance in rice (Zhang et al., 2017) (Figure 1). This OsbHLH002/OsICE1 pathway targeting MAPK3 in rice mainly affects trehalose synthesis and metabolism, thus representing a new regulatory pathway. In addition, recent studies have found that CRPK1 (Cold-responseive protein kinases 1), a membrane-specific cold responsive protein kinase, negatively regulates the freezing resistance of Arabidopsis thaliana by phosphorylating 14-3-3 protein, transferring cold signals from plasma membrane to nucleus, accelerating E3 ubiquitination degradation of CBF1 and CBF3 (Liu et al., 2017) (Figure 1). This study has opened up a new regulatory model independent of MPK phosphorylation pathway.

Cold stress activated protein kinase OST1 (Open stomata 1) is a SnRK family protein kinase that regulates stomatal opening and closing in ABA signal (Ding et al., 2015). It was found that Arabidopsis OST1 blocked the ubiquitination of ICE1 by HOS1 through phosphorylation of ICE1 at Ser278 site, thereby positively regulating CBF-mediated freezing tolerance in Arabidopsis (Figure 1). In addition, OST1 can also phosphorylate transcription factors of NAC (A nascent polypeptide-associated complex), BTF3 (Basic transcription factor 3) and BTF3L (BTF-like) in Arabidopsis. In which, phosphorylated BTF3s up-regulated CBFs expression and protein stability by interacting with CBF proteins, thereby improving plant freezing resistance (Ding et al., 2018) (Figure 1). Interestingly, protein phosphatase EGR2 (Glade E growth-regulating 2) is also involved in the regulation of OST1 activity (Ding et al., 2019). Under cold stress, the interaction between EGR2 and NMT1 (N-myristoyltransferase) was weakened, thereby inhibiting the myristoylation of EGR2. The newly synthesized non-myristoylation EGR2 (u-EGR2) decreased the binding ability to OST1, resulting in the release of EGR2-mediated inhibition of OST1 activity, thereby enhancing the freezing resistance of plants (Ding et al., 2019) (Figure 1).

3.2 Ubiquitination and SUMO regulation

RING E3 ligase OsHOS1 mediated the ubiquitination of ICE1 (Dong et al., 2006). Overexpression of HOS1 in Arabidopsis thaliana resulted in down-regulation of CBF3 expression and decreased freezing resistance of plants (Dong et al., 2006). Similarly, rice OsICE1 can also be degraded by OsHOS1 (Zhang et al., 2017). In a word, Arabidopsis, and rice MYB transcription factors are important transcription factors for plant cold stress. Arabidopsis MYB15 negatively regulates plant freezing resistance by inhibiting CBFs expression (Agarwal et al., 2006). Recent studies have shown that two U-box E3 ligases PUB25 and PUB26 can mediate ubiquitination degradation of MYB15, thereby positively regulating freezing resistance of Arabidopsis. Recent studies have shown that two U-box E3 ligases PUB25 and PUB26 can mediate ubiquitination degradation of MYB15, thereby positively regulating freezing resistance of Arabidopsis (Wang et al., 2019) (Figure 1). Under cold stress, activated OST1 phosphorylated PUB25 and PUB26, thereby enhancing their E3 ligase activity to degrade MYB15 (Wang et al., 2019). On the contrary, SUMO modification can protect the target protein from ubiquitination degradation. Arabidopsis SIZ1 (SAP and Miz) encodes a SUMO E3 ligase, which enhances the stability of ICE1 by mediating the SUMOylation of Lys393 site of ICE1, and effectively inhibits the ubiquitination and degradation of ICE1 by HOS1, thus maintaining the high expression regulation of CBF-COR by ICE1 (Miura et al., 2007) (Figure 1).

4 Epigenetic Regulation of Cold Signaling Pathway

Epigenetic regulation is also involved in the regulation of gene expression in the cold signaling pathway. Arabidopsis has two miR397 subtypes: miR397a and miR397b (Sunkar and Zhu, 2004). In which, overexpression of miR397a increased the tolerance of Arabidopsis to chilling and freezing stresses (Dong and Pei, 2014). Although the expression level of CBF-COR in mi397a overexpression plants was significantly higher than that in wild type, the direct target of miRNAs is unclear (Dong and Pei, 2014). SICKLE (SIC) is a proline-rich protein involved in Arabidopsis development and abiotic stress tolerance. SIC colocalizes with HYL1 (Hyponastic leaves 1), a biosynthetic component of miRNAs, and participates in the biosynthesis and intron degradation of some miRNAs (Zhan et al., 2012). Compared with the wild type, the levels of miRNA and siRNA in sic-1 mutation were lower, and the sensitivity to cold and salt stress was increased (Zhan et al., 2012).

HATs (Histone acetyltransferases) and HDAs (Histone deacetylases) are closely related to gene expression under cold stress (Kim et al., 2015). Arabidopsis GCN5 (General control non-derepressible 5) is a kind of HAT. Compared with the wild type, the gcn5 mutant showed delayed induction of CORs and decreased expression level, indicating that GCN5 positively regulated the freezing resistance of Arabidopsis thaliana by regulating the histone acetylation of CORs (Vlachonasios et al., 2003). In maize, low temperature up-regulated the expression of HDAs, resulting in the hyperacetylation of H3 and H4 and the activation of the expression of cold-induced genes ZmDREB1 and ZmICE1 (Hu et al., 2011). In addition, low temperature also induced the expression of HDA6 in Arabidopsis thaliana and participated in the regulation of freezing resistance (To et al., 2011). In terms of deacetylation, the histone deacetylation of Arabidopsis WD40 repeat protein HOS15 may be related to plant freezing resistance (Zhu et al., 2008). However, how HOS15 regulates CORs is unclear. Recent studies have shown that HOS15 activates the expression of CORs (COR47 and COR15A) by interacting with HD2C (Park et al., 2018). Under normal temperature, HOS15-HD2C complex binds to the CORs promoter and inhibits the expression of CORs by inducing deacetylation of CORs chromatin. Under cold stress, HOS15 ubiquitinated HD2C by activating E3 ligase CUL4 (CULLIN4), thus enhancing the binding ability of CBFs to CORs promoter (Park et al., 2018).

5 Discovery of Cryogenic Signal Sensor

Low temperature induces changes in cell membrane fluidity and cytoskeleton rearrangement, triggering calcium influx and activating the expression of downstream CORs, which is the main model of plant cold induction mechanism (Zhu, 2016). TRP (Transient receptor protential) superfamily is involved in mammalian thermal response (Venkatachalam and Montell, 2007). However, TRP homologous proteins are not found in terrestrial plants. Therefore, whether calcium channels are directly involved in plant perception of cold signals has been a mystery. Recently, studies on the genetic populations of cold-sensitive indica rice 9311 and cold-tolerant japonica rice Nipponbare found that transmembrane protein COLD1 was involved in the response of rice to low temperature (Ma et al., 2015). COLD1 regulates G protein signal by interacting with RGA1 (Rice-protein α subunit 1), thus accelerating GTPase activity (Ma et al., 2015) (Figure 1). COLD1-RGA1 complex mediates Ca²⁺ influx and activates downstream CORs expression under chilling stress (Ma et al., 2015). Therefore, COLD1 may be a potential Ca²⁺ permeation channel or a direct regulator of such channels. However, whether the Ca²⁺ influx mediated by COLD1 alone can fully activate the cold tolerance of plants, and whether there are other Ca²⁺ channels (CNGCs) involved in the perception of cold signals will be an interesting topic (Ma et al., 2015).

6 Summary and Prospect

CBF-COR pathway represents the key components of cold signaling pathway and is positively or negatively regulated at different levels. However, only about 10%~25% of CORs were regulated by CBFs (Park et al., 2015; Jia et al., 2016; Zhao et al., 2016), indicating that some CBF-independent transcription factors were also involved in the regulation of CORs expression. For example, HSFC1 (Heat shock transcription factor 1), ZAT10/12 (Zinc finger of Arabidopsis thaliana 10/12), CZF1 (Cold-inducible zinc finger 1), ZF (Zinc finger transcription factor), RAV1 (Related to ABI3/VP1 transcription factor) and HY5 (Elongated hypocotyl 5) regulate the expression of CORs by bypassing CBF signals (Vogel et al., 2005; Park et al., 2015), indicated that overlapping and parallel regulation existed among different cold response pathways, and how these transcription factors fine-tune the expression of CORs to establish cold acclimation remains to be further studied.

Cold stress increases intracellular Ca²⁺ levels. However, whether Ca²⁺ channels are directly involved in the induction of low temperature and how Ca²⁺ signaling is induced under low temperature still unclear. Although several protein kinases have been successfully identified to participate in CBF signal transduction, how early low temperature activates these protein kinases remains to be studied. Considering that COLD1 may regulate intracellular Ca²⁺ levels (Ma et al., 2015), establishing the relationship between Ca²⁺ signaling and kinase activity will be the focus of future research.

The overexpression of CBFs led to plant dwarfing and biomass reduction (Gilmour et al., 2000; Achard et al., 2008), while the plant type of cbfs tertiary mutant was larger than that of the wild type under cold stress (Jia et al., 2016), indicating that CBFs may be an important regulator to balance plant growth and cold response. Low temperature is one of the most frequent stresses of environmental change, which requires plants to balance and coordinate the integration of internal and external signals throughout the life cycle to respond to changing environments. Recent studies have found that to protect roots from cold damage, cold stress can lead to the death of capsular stem cells, thereby inducing DNA damage of root stem cells and preventing further division of stem cells (Jing et al., 2017). In addition, cold-tolerant species had higher stomatal index and stomatal frequency than non-cold-tolerant species (Palta and Li, 1979). Interestingly, OST1 and ICE1 are mainly located in stomata (Mustilli et al., 2002; Kanaoka et al., 2008). Vascular tissue may also be an important part of plant response to cold stress, and key cold signal regulators such as OST1 and BTF3s are also located in the vascular tissue of roots and leaves (Mustilli et al., 2002; Ding et al., 2018). A better understanding of the balance between organogenesis and cold response at the molecular level is helpful to improve the survival ability of plants during and/or after cold stress.

The development and cultivation of cold-tolerant crop varieties is helpful to expand the planting area to high latitudes and high altitudes. Among them, transgenic is one of the important strategies to improve crop cold tolerance. In addition, using high-density population and genome-wide association analysis to identify quantitative trait loci or natural variations is another way. COLD1 is the basis of QTLs for cold tolerance in rice, and has little interaction with other QTLs, which is a useful feature in breeding gene operation. COLD1 has 7 SNP. Among them, SNP2 showed specificity among subspecies, including A in japonica rice and C/T in indica rice. The SNP2 molecular module of COLD1^jap can be used in cold tolerance breeding of rice (Ma et al., 2015). The near isogenic lines carrying COLD1^jap allele not only showed strong cold tolerance, but also maintained their yield. In addition, overexpression of OsMADS57 could maintain the tiller growth of rice under chilling stress (Chen et al., 2018). OsMADS57 contains genomic fragments with natural function acquired mutations, which can be used as another potential cold tolerance module. The integration of OsMADS57 module and COLD1^jap module is expected to improve rice cold tolerance while maintaining or even increasing field yield, which provides an effective solution to solve the contradiction between high yield and cold tolerance.

Authors’ contributions

CJJ and FW are the main writers of the review, completing the collection and analysis of relevant literature and the writing of the first draft of the paper. LH, ZHL, and HZH participated in the analysis and collation of literature. HMR and FW are the project designer and director, guiding manuscript writing and revision. All authors read and approved the final manuscript.

Acknowledgments

This study was supported by the Major Science and Technology Projects in Yunnan Province (2017ZF004) and "Ten Thousand Talents Program" for Young Top-notch talents in Yunnan Province (YNWR-QNBJ-2018-047).

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