Review Article | Open Access
Roles of C-Repeat Binding Factors-Dependent Signaling Pathway in Jasmonates-Mediated Improvement of Chilling Tolerance of Postharvest Horticultural Commodities
C-repeat binding factor- (CBF-) dependent signaling pathway is proposed to be a key responder to low temperature stress in plant. Jasmonates (JAs), the endogenous signal molecules in plant, participate in plant defense against (a)biotic stresses; however, the mechanism has not been fully clarified so far. With the progress made in JAs biopathway, signal transduction, and their relationship with CBF-dependent signaling pathway, our knowledge of the roles of the CBF-dependent signaling pathway in JAs-mediated improvement of chilling tolerance accumulates. In this review, we firstly briefly review the chilling injury (CI) characteristics of postharvest horticultural commodities, then introduce the biopathway and signal transduction of JAs, subsequently summarize the roles of the CBF-dependent signaling pathway under low temperature stress, and finally describe the linkage between JAs signal transduction and the CBF-dependent signaling pathway.
Preservation, transportation, and marketing of postharvest horticultural commodities at low temperatures constitute the main strategy employed in food industries to retard quality deterioration . However, upon exposure to low temperatures ranging from 0 to 15°C, a series of physiological and biochemical alternations is initiated in some horticultural commodities of tropical/subtropical origin, leading to the development of chilling injury (CI) and a great economical loss [2–5].
During low temperature stress, cold signal is perceived by undefined sensor in membrane prior to the activation of several cold signaling pathways . In the promoters of these genes, there are cis-elements termed C-repeat elements/dehydration-responsive elements (CRT/DRE), where C-repeat binding factors (CBFs) bind . CBFs, which participate in transcriptional regulation of low temperature acclimation , are under the positive control of the upstream Inducer of CBF Expression (ICE), including ICE1 and ICE2 . Activation of CBF-dependent signaling pathway, particularly the ICE1-CBF transcriptional cascade, is proposed to be a key response to low temperature stress in plant, enhancing their chilling resistance [6, 9]. Three CBFs, which are involved in low temperature stress, have been identified in Arabidopsis, including AtCBF1, AtCBF2, and AtCBF3 . Overexpression of AtCBF2 results in the induction of 85 cold-regulated (COR) genes in Arabidopsis .
Jasmonic acid and its derivatives, collectively referred to as jasmonates (JAs), are ubiquitous plant hormone . Besides functioning in plant growth and developmental process, JAs play important roles in plant defense against a variety of (a)biotic stresses, such as pathogens , herbivory , mechanical wounding , low temperature , and high salinity .
The roles of JAs in alleviating the CI of postharvest horticultural commodities have been the focus of research for many years. Upon exposure to (a)biotic stresses, the increase of endogenous JAs precedes the activation of JAs-mediated defense ; meanwhile, the application of exogenous JAs at proper concentrations could effectively ameliorate CI symptoms of postharvest horticultural commodities, such as papaya, avocado, banana, and tomato (Table 2), and this effect might be due to the activation of various physiological and biochemical responses . However, this mechanism has not yet been fully clarified. With the aid of new technologies, our knowledge on JAs biosynthesis, signal transduction, and their relationship with CBF-dependent signaling pathway expands. In this review, we firstly briefly review the CI characteristic of postharvest horticultural commodities, then introduce the biopathway and signal transduction of JAs, subsequently summarize the roles of CBF-dependent signaling pathway during the low temperature stress, and finally describe the linkage between JAs signal transduction and the CBF-dependent signaling pathway. This review would provide a deeper understanding on the mechanism employed by prechilling JAs treatment to mitigate CI of postharvest horticultural commodities.
2. CI Characteristics of Postharvest Horticultural Commodities
2.1. CI Symptoms and Impact Factors
Exposure of horticultural commodities of tropical/subtropical origin to low temperature ranging from 0 to 15°C would initiate a series of physiological and biochemical alternations, leading to the development of various CI symptoms [2–4], which can be categorized into two groups: (1) developmental or metabolic symptoms with qualitative nature and (2) physiological symptoms, including pitting, discoloration, water soaking, internal breakdown, susceptibility to mechanical injury, and fungal attack . Table 1 lists CI symptoms of several horticultural commodities along with their critical chilling temperatures .
Many factors can impact the chilling susceptibility of horticultural commodities, including the genotype, ripening stage, metabolic status, and other environmental conditions . For example, green and breaker tomato fruits (<10% red coloration, USDA 1976) are more susceptible to low temperature stress than fruits at red-ripe stage . A more severe CI phenomenon was observed in horticultural commodities subjected to lower environmental temperatures. Additionally, the duration of chilling exposure is positively correlated with CI index .
However, it is the genetic makeup that determines to what degree a species or cultivar is sensitive or resistant to low temperature stress . Arabidopsis with higher expression level of AtCBF3 demonstrates an enhanced chilling tolerance .
2.2. Physiological and Biochemical Alternations Resulting in the Development of Visual CI
The cell membrane is the primary cellular structure affected by low temperature stress . The transition of cell membrane from a liquid-crystalline phase to a solid-gel structure during chilling stress causes the loss of membrane semipermeability, the dysfunction of membrane proteins, the increase of free cytosolic calcium, and the cessation of protoplasmic streaming, which is followed by the electrolyte leakage, energy supply reduction, and an increase in susceptibility to oxidative stress [55, 56] (Figure 1). If there is exposure to chilling stress for a longer time, further responses could be initiated along with the rupture of cell membrane, presenting as various visual CI symptoms such as pitting, water soaking, and decay [3, 4] (Figure 1).
3. Biopathway and Signal Transduction of JAs
3.1. JAs Biosynthetic Pathway
As shown in Figure 2, JAs biosynthesis is initiated by a phospholipase-mediated release of α-linolenic acid in chloroplast, which is then oxidized by TomloxD into 13(S)-hydroperoxylinolenic acid (13-HPOT) [57, 58]. The latter is further oxidized and cyclized into cis-(+)-12-oxophytodienoic acid (cis-(+)-OPDA) by the actions of allene oxide synthase (AOS) and allene oxide cyclase (AOC) . Subsequently, cis-(+)-OPDA is transported by COMATOSE1/PEROXIMAL1/PEROXISOME ABC TRANSPORTER (ABC CTS1/PXA1/PED3) or ion trapping from the chloroplast to the peroxisome , where cis-(+)-OPDA is oxidized and then esterified before three rounds of β-oxidation with the generation of (+)-7-iso-JA . The core enzymes for β-oxidation include acyl CoA oxidase (ACX), multifunctional protein (MFP), and 3-ketoacyl-CoA thiolase (KAT) . Upon synthesis, the (+)-7-iso-JA is immediately epimerized to (−)-JA and further converted into various derivatives, such as methyl jasmonate (MeJA) and jasmonoyl-isoleucine (JA-Ile) [58, 62] (Figure 2). In plant, a small amount of JAs is derived from hexadecatrienoic acid .
JAs biosynthesis in plant is regulated by various factors, like substrate availability, JASMONATE-ZIM-DOMAIN (JAZ) protein, Ca2+/mitogen-activated protein kinase (MAPK) cascades, and so on . Among several branches known for the LOX pathway, the AOS and hydroperoxide lyase (HPL) branches are concurrent on the same substrate, 13-HPOT . The HPL branch leads to the generation of green leaf volatiles (GLVs), which are defense compounds formed upon herbivore attack [64, 65]. Mutation of OsHPL3 would reduce wound-induced GLV emission but increase JAs accumulation . For more information relevant to the regulation of JAs biosynthesis, readers could refer to the review written by Wasternack and Hause .
3.2. JAs Signal Transduction
Recently, JA-Ile has been identified as the bioactive compound in JAs signaling . Along with this discovery, other breakthroughs relevant to JAs signal transduction have been made, such as the identification of JAZ repressors [67, 68] and CORONATINE INSENSITIVE1-JAZ (COI1-JAZ) coreceptor .
Figure 3 summarizes the primary signal transduction process after its perception [58, 71, 72]: in the absence of JA-Ile, JAZ repressors suppress transcription factors (TFs) such as bHLHzip transcription factors (MYCs) by recruiting the corepressors TOPLESS (TPL) and TPL-related proteins via the adaptor protein, Novel Interactor of JAZ (NINJA), and thus suppress the expression of JAs-regulated genes. On the other hand, during plant development or (a)biotic stresses when JA-Ile levels are high, a F-box protein COI1, which is an integral part of the Skp-Cullin-F-box (SCF) complex, targets JAZ repressors by the aid of inositol pentakisphosphate 5 (IP5) for poly-ubiquitination; JAZ repressors are subsequently degraded by a 26S ubiquitin-proteasome system, thus relieving TFs blockage and activating the gene expression downstream [19, 73]. The initiation of transcription also needs the recruitment of general transcription factors (GTFs) and RNA polymerase II to TFs-bound promoter through the interaction of TFs and MEDIATOR25 (MED25) subunit of Mediator complex  (Figure 3).
4. Exogenous Application of JAs to Reduce CI of Postharvest Horticultural Commodities
Upon exposure to (a)biotic stresses, the increase of endogenous JAs precedes the activation of JAs-mediated defense . A higher level of endogenous JA was observed in the skin of mangosteen during early storage at 7°C , which agreed with the finding in apple fruitlet . These results imply a role of JAs in low temperature stress of postharvest horticultural commodities. Table 2 lists the reports on exogenous JAs application ameliorating CI symptoms of postharvest horticultural commodities, such as papaya, avocado, banana, tomato, bell pepper, grapefruit, guava, and loquat. The fumigation of “Sunrise” papaya with 0.01 or 0.1 mM MeJA vapors for 16 h significantly suppressed CI symptoms, such as fungal decay, surface pitting, and loss of firmness, after 32 d storage at 10°C + 4 d shelf life at 20°C .
Based on the report of Aghdam and Bodbodak , the JAs-mediated chilling alleviation of postharvest horticultural commodities could be due to the physiological and biochemical responses as follows: (1) enhancement of membrane integrity through the increase of unsaturated fatty acids/saturated fatty acids (unSFA/SFA) ratio; (2) enhancement of heat shock proteins (HSPs) gene expression; (3) enhancement of reactive oxygen intermediates- (ROIs-) scavenging capacity; (4) enhancement of arginine pathways, resulting in the accumulation of bioactive molecules with pivotal roles in chilling resistance; (5) enhancement of energy metabolism, leading to more adenosine triphosphate (ATP) accumulation; (6) alteration in phenylalanine ammonia-lyase (PAL) and polyphenol oxidase (PPO) activities (Table 2).
Cultivar, ripening stage, and JAs dosage can impact the efficiency of JAs treatment [20, 25]. Ding et al.  found that a 0.1 mM MeJA fumigation of breaker “Beefsteak” tomato prior to 28 d storage at 5°C substantially inhibited the development of surface pitting and Alternaria decay; however, this concentration was not effective for pink fruit . Although 0.037, 0.074, or 0.110 mM MeJA fumigation could effectively suppress pitting, browning, and water loss during low temperature storage of “Malas Save” pomegranate fruits, the optimal result was observed in fruits treated with the highest concentration .
5. Roles of CBF-Dependent Signaling Pathway during Low Temperature Stress
5.1. Activation of CBF-Dependent Signaling Pathway during Low Temperature Stress
Upon exposure to low temperature, plants immediately activate multiple signaling pathways to enhance chilling tolerance, which consists of transcriptional, posttranscriptional, translational, and posttranslational regulators of low temperature-induced expression of the functional genes . In the promoters of these genes, there is a kind of cis-elements termed C-repeat elements/dehydration-responsive elements (CRT/DRE), where CBFs can bind . CBFs, which participate in transcriptional regulation of low temperature acclimation , are under the positive control of the upstream ICEs, including ICE1 and ICE2 . Activation of CBF-dependent signaling pathway, especially the ICE1-CBF transcriptional cascade, is supposed to be a key responder to low temperature stress in plant, enhancing their chilling resistance [6, 9]. Chilling stress results in the induction of OsICE1 and OsICE2 in rice (Oryza sativa) and subsequent upregulation of OsCBF1, rice heat shock factor A3 (OsHsfA3), and rice trehalose 6-phosphate phosphatase 1 (OsTPP1) expression . Overexpression of SlICE1 in tomato fruit initiates the expression of SlCBF1, dehydrin Ci7 homolog (SlDRCi7), and pyrroline-5-carboxylate synthetase (SlP5CS) and enhance the accumulation of antioxidants, several amino acids, amines, and sugars, thus improving the chilling resistance of fruit [81, 82]. A similar result was observed in cucumber .
In Arabidopsis, three CBFs—namely, AtCBF1, AtCBF2, and AtCBF3—have been identified to be involved in low temperature stress . Under normal condition, JAZ1 and JAZ4 in Arabidopsis would interact with ICEs, thus suppressing CBF-dependent signaling pathway . Upon low temperature acclimation when the biosynthesis of endogenous JAs is induced, ICE1 is released from the JAZs via a 26S proteasome-mediated degradation and then positively regulates the expression of CBFs . Subsequently, CBFs bind to CRT/DRE in CORs and upregulate their expression, which could induce the physiological and biochemical responses and thus improve chilling tolerance of plant . For the detailed information on the roles of CBF-dependent signaling pathway in chilling acclimation, readers could refer to the reviews on this topic [6, 85, 86].
5.2. Physiological and Biochemical Responses Induced by CBF-Dependent Signaling Pathway to Improve Chilling Tolerance
5.2.1. Enhancing Arginine Pathways
Arginine is a precursor for the biosynthesis of bioactive molecules such as polyamines, proline, and γ-aminobutyric acid [36, 52] (Figure 4). Polyamines could stabilize the membrane based on its polycationic nature at physiological pH , proline acts as a protein-compatible hydrotrope or as a hydroxyl radical scavenger to regulate the NAD+/NADH ratio , while γ-aminobutyric acid is involved in osmotic regulation, ROS scavenge, and intracellular signal transduction .
As shown in Figure 4, in plant arginase is metabolised by arginase (ARG), ornithine decarboxylase (ODC), and arginine decarboxylase (ADC) with ornithine and agmatine as intermetabolites . Ornithine could also be converted into γ-aminobutyric acid by P5CS and glutamate decarboxylase (GAD) or into proline by pyrroline-5-carboxylate reductase (P5CR) (Figure 4) [36, 52].
CBF-dependent signaling pathway plays a pivotal role in arginine metabolism. Tomato with upregulated expression of SlICE1 showed higher expression levels of SlP5CS and higher concentrations of polyamines, proline, and γ-aminobutyric acid, thus improving the chilling tolerance of fruit [81, 82]. A similar phenomenon was observed by the overexpression of AtCBF3/DREB1A in Arabidopsis .
5.2.2. Enhancing ROIs-Scavenging Capacity
ROIs are the partially reduced forms of O2 . Chilling exposure could stimulate the production and overaccumulation of ROIs, which disrupts the cellular homeostasis and cause cell death [77, 91]. In plant, the major ROIs-scavenging pathways consist of (i) water-water cycle; (ii) ascorbate-glutathione cycle; (iii) glutathione-peroxidase (GPX) cycle; and (iv) catalase (CAT)  (Figure 5). Among these, the ascorbate-glutathione cycle plays a crucial role in regulating ROIs based on its wide distribution as well as the high affinity of ascorbate peroxidase (APX) for H2O.
ROIs-scavenging capacity in plant is correlated with CBF-dependent signaling pathway. Overexpression of SlICE1 in tomatoes could enhance the accumulation of antioxidants, such as β-carotene, lycopene, and ascorbic acid, as well as antioxidant activity, thus improving the chilling tolerance of tomato [81, 82].
5.2.3. Enhancing Energy Metabolism
Energy supply is also very important during the stress response as an ATP deficit would induce membrane lipid peroxidation and subsequently generate more free radicals, which would attack the cellular membrane [92, 93]. In plant, ATP is synthesized from glucose by a series of pathways, including glycolysis, Kreb’s cycle, electron transfer chain, and oxidative phosphorylation.
CBF-dependent signaling pathway is supposed to be involved in energy metabolism. Overexpression of SlICE1 in tomato enhanced the accumulation of metabolites relevant to ATP generation, such as glucose, fructose, glucose 6-phosphate, fructose 1,6-diphosphate, phosphoenolpyruvate, citric acid, and succinic acid, thus improving the chilling tolerance of tomato [81, 82]. Similarly, overexpression of the AtCBF3 could enhance the chilling tolerance of Arabidopsis, which was associated with higher abundances of glucose and fructose .
5.2.4. Enhancing the Expression of HSPs
HSPs, a stress-responsive family of proteins with molecular weight between 15 and 115 kDa, are comprised of five subfamilies, including HSP70s, HSP60s, HSP90s, HSP100s, and small HSPs (sHSPs) . They are widely distributed within cellular compartments and exert their protective role against stress based on molecular chaperone activity to sustain protein trafficking as well as maintain the integrity and function of the cell membrane [7, 94]. Furthermore, sHSPs can exert molecular chaperone activity independent of ATP .
The expression levels of HSPs genes are regulated by the CBF-dependent signaling pathway [96, 97]. Previously, Nakamura et al.  found that chilling stress caused the induction of OsICE1 and OsICE2 in rice and subsequent upregulation of OsCBF1, OsHsfA3, and OsTPP1 expression.
6. Linkage between JAs Signal Transduction and CBF-Dependent Signaling Pathway
Although several physiological and biochemical responses are observed after JAs treatment, the mechanism has not been clarified until recently. Activation of the CBF-dependent signaling pathway, especially the ICE1-CBF transcriptional cascade, is proposed to perform a large duty during JAs-induced chilling tolerance. Previously, Zhao et al.  observed that MYC2 was involved in JAs-induced chilling tolerance through physical interaction and functional coordination with ICE1, regulating the CBF-dependent signaling pathway. In association with the higher expression of MaMYC2a and MaMYC2b after dipping “Carvendish” banana in 0.1 mM MeJA solution for 30 min was the enhanced expression of MaCBF1, MaCBF2, and CBF downstream genes, including COR1, KIN2, RD2, and RD5 . Since MYC2 is one of the TFs in JAs signal transduction pathway, these results imply a potential linkage between two signal transduction pathways. Furthermore, various physiological and biochemical responses induced by CBF-dependent signaling pathway were also observed in postharvest horticultural commodities after JAs treatment (see Sections 4 and 5).
In combination with previous reports [6, 9, 78, 84], the primary signal transduction process after prechilling JAs treatment to activate CBF-dependent signaling pathway in order to improve the chilling resistance of postharvest horticultural commodities is illustrated in Figure 6: higher JAs content after prechilling JAs treatment triggers COI1-mediated degradation of JAZs, releasing MYC2 and ICE1 from repression. MYC2 and ICE1 then interact with each other to activate the expression of CBFs, which subsequently bind to the CRT/DRE box promoter sequence element to induce the expression of CBF downstream genes, such as CORs . The induction of CORs expression needs SENSITIVE TO FREEZING 6 (SFR6) to recruit RNA polymerase II to the promoter . Following this is the initiation of the gene expression downstream, which subsequently induces various physiological and biochemical responses, resulting in the improvement in the chilling tolerance of postharvest horticultural commodities.
7. Conclusions and Perspectives
Activation of CBF-dependent signaling pathway, especially the ICE1-CBF transcriptional cascade, is proposed to be a key response to low temperature stress in plant, enhancing their chilling tolerance [6, 9].
Prechilling JAs treatment shows a potential to alleviate the CI of postharvest horticultural commodities. However, our understanding of its mechanism is still rudimentary. In association with new discoveries in JAs biosynthesis, signal transduction, and the roles of the CBF-dependent signaling pathway during chilling stress, the linkage between JAs signal transduction and CBF-dependent signaling pathway is identified. This review summarizes the previous studies relevant to JAs and CBF-dependent signaling pathway and further proposed the primary signal transduction process after JAs treatment to activate CBF-dependent signaling pathway to enhance the chilling tolerance (Figure 6). However, there are still some questions which need to be addressed, such as the roles of other MYCs (except for MYC2) in the activation of CBF-dependent signaling pathway.
In addition, according to microarray and real-time analysis of wild-type Arabidopsis and its coi1 mutant, Hu et al.  observed that transcriptional levels of some CORs, which were not induced by CBF-dependent signaling pathway, were lower in coi1 mutant upon low temperature exposure. These results suggest that some physiological and biochemical responses might result from CBF-independent signaling pathway . Thus, further work is needed to clarify the roles of the physiological and biochemical responses induced by the CBF-independent signal pathway and their roles in JAs-mediated chilling resistance with the aid of genomics, proteomics, transcriptomics, and metabolomics, which will give us a more comprehensive understanding on the mechanism employed by exogenous JAs application to mitigate CI symptoms of postharvest horticultural commodities.
Conflicts of Interest
The authors have declared that no conflicts of interest exist regarding the publication of this paper.
Libin Wang wrote the paper; Weiqi Luo, Xiuxiu Sun, and Chunlu Qian searched and collected the material.
The authors would like to thank the National Natural Science Foundation of China (31701868), the Fundamental Research Funds for the Central Universities (Y0201700670), Public Welfare Research Projects of the Ministry of Agriculture of China (2014030232), and Metabolomic & Microbial Profiling of Tropical/Subtropical Fruits and Small Fruits for Quality Factors and Microbial Stability (6034-41430-005-00) for the financial support of this study. Meanwhile, they thank Dr. Christopher Ference (Horticultural Research Laboratory, Fort Pierce, Florida, USA) for English language editing and Shaoling Zhang for providing some advice for manuscript construction and some financial support.
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