Submitted Successfully!
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Ver. Summary Created by Modification Content Size Created at Operation
1 -- 4810 2023-11-20 10:06:59 |
2 format change Meta information modification 4810 2023-11-20 10:18:15 |

Video Upload Options

Do you have a full video?


Are you sure to Delete?
If you have any further questions, please contact Encyclopedia Editorial Office.
Caccialupi, G.; Milc, J.; Caradonia, F.; Nasar, M.F.; Francia, E. Triticeae CBF Gene Cluster for Frost Resistance. Encyclopedia. Available online: (accessed on 28 November 2023).
Caccialupi G, Milc J, Caradonia F, Nasar MF, Francia E. Triticeae CBF Gene Cluster for Frost Resistance. Encyclopedia. Available at: Accessed November 28, 2023.
Caccialupi, Giovanni, Justyna Milc, Federica Caradonia, Muhammad Fazail Nasar, Enrico Francia. "Triticeae CBF Gene Cluster for Frost Resistance" Encyclopedia, (accessed November 28, 2023).
Caccialupi, G., Milc, J., Caradonia, F., Nasar, M.F., & Francia, E.(2023, November 20). Triticeae CBF Gene Cluster for Frost Resistance. In Encyclopedia.
Caccialupi, Giovanni, et al. "Triticeae CBF Gene Cluster for Frost Resistance." Encyclopedia. Web. 20 November, 2023.
Triticeae CBF Gene Cluster for Frost Resistance

The pivotal role of CBF/DREB1 transcriptional factors in Triticeae crops involved in the abiotic stress response has been highlighted. The CBFs represent an important hub in the ICE-CBF-COR pathway, which is one of the most relevant mechanisms capable of activating the adaptive response to cold and drought in wheat, barley, and rye. Understanding the intricate mechanisms and regulation of the cluster of CBF genes harbored by the homoeologous chromosome group 5 entails significant potential for the genetic improvement of small grain cereals. 

abiotic stress Triticeae CBF transcription factors cold acclimation frost tolerance drought tolerance

1. Triticeae as Staple Food and Adaptable Crops

The Green Revolution had been able to meet the demand for food, reducing world hunger among the growing population (from 2.519 billion in 1950 to 4.435 billion in 1980) thanks to an unprecedented increase in crop yield and agricultural production [1][2]. New irrigation techniques, massive use of fertilizers and plant protection products, mechanization, crop breeding, and adoption of improved varieties were the determining factors in the observed increase in productivity [3][4][5]. Cereal crops, in particular, saw significant improvement, with yields tripling despite a small increase in arable land [6][7]. However, besides the positive effects, the excessive agricultural intensification created the conditions for the rise of environmental problems such as pollution, soil degradation, and loss of genetic diversity [8][9]. For example, in many breeding programs, genotypes were selected for the high-input systems driving gene pool erosion, especially for the alleles responsible for adaptation to the environment [10][11][12]. However, new issues emerged: yield seems to have reached a plateau and a contraction of genetic diversity has been observed [13][14]; as a result, the adaptation to biotic and abiotic stresses of cereal crops has been reduced [15][16][17][18][19]. In a scenario where the population is still growing (based on UN estimations, planet Earth will be populated by 8.5, 9.7, and 10.9 billion people by 2030, 2050, and 2100, respectively [2]), one of the goals of the global food production system is to provide higher yields and food quality while reducing, however, environmental pollution [6]. Furthermore, extreme weather conditions, reduction of arable lands, and increasing demand of fertilizers and irrigation water are putting the crops cultivation in open fields under stress conditions, significantly affecting agricultural production on all continents [20]. A novel approach is required to cope with the climate issue. Crop breeding programs need to develop new genotypes with a higher adaptation to weather fluctuations [21][22] and contribute to global food security [23].
The Triticeae tribe, a grass tribe of the Poaceae family that includes cultivated wheats (durum wheat Triticum turgidum L. ssp. durum Desf., bread wheat Triticum aestivum L.), barley (Hordeum vulgare L.), and rye (Secale cereale L.), is by far the most important source of energy and nutrients worldwide [24][25]. For example, wheat and barley together were the most cultivated herbaceous crops in the world in 2021, with a harvested area of 220 and 48 million hectares and a total grain production of 770 and 145 million tons, respectively [26]. Rye is an important crop for Northern and Eastern European countries, with a harvested area of 3.5 million hectares and a total production of 11 million tons [26]. The Triticeae tribe comprises about 350 species, including the so-called minor cereals such as triticale, spelt emmer, and einkorn wheats, poulard, polish, and khorasan wheats [27].
Temperate grass species are characterized by winter growth habits (WH) in their natural environments [28][29]. The two key traits of WH genotypes are the vernalization requirement and the cold acclimation. Vernalization is defined as the induction of flowering after prolonged exposure to cold. Moreover, Triticeae are usually classified as long-day (LD) plants because most varieties flower earlier when exposed to longer days. This mechanism synchronizes plants to flower after cold, harmful temperatures in the wintertime [30][31]. The cold acclimation is the ability of the crop to adapt to cold temperatures and then survive frost events [32]. The winter habit (WH) genotypes are usually sown in winter due to their higher productivity. In Mediterranean climates, sowing is performed in the autumn to take advantage of the rainiest seasons, and the plants are harvested during the drier summer. Winter habit is a limiting factor in the widespread cultivation of Triticeae in environments where winter is too cold to survive or too warm to satisfy the vernalization requirement [33]. To overcome this limit, spring habit (SH) and facultative habit (FH) genotypes were selected for their lack of vernalization requirements [34][35]. SH genotypes are sown in spring, whereas FH genotypes can be alternatively sown either in autumn or spring. Most SH cultivars are frost-prone and, due to a shorter crop cycle, may be exposed to drought. For these reasons, in the last few years, FH genotypes are gaining more and more interest since they show a high level of frost tolerance (FT) and do not require vernalization [36][37]. The Triticeae crops are thus adaptable to several environments, ranging from sub-arctic to tropical climates, allowing their cultivation across a wide geographical area [38][39], even if the highest yields are achieved in temperate regions [40].

2. C-Repeat Binding Factors and Cluster Organization in Triticeae

C-repeat binding factors, or dehydration responsive element (CBF/DREB1), are a larger subfamily of transcription factors that belong to the APETALA2/ethylene-responsive element binding factor (AP2/ERF) protein family and are induced/activated in response to osmotic stresses such as cold or drought. The AP2/ERF domain binds to the C-repeat/dehydration responsive elements (CRT/DRE) in the promoter region of a variety of genes involved in the abiotic stress response, also known as “CBF’s regulon.” These genes protect against the adverse effects of losing water caused by frost and drought with the biosynthesis of osmoprotectant proteins, carbohydrate metabolism-related activity, and sugar transport [41][42][43]. Among these, cold-regulated genes (COR) are the most important family, including late embryo abundant proteins (LEA), low-temperature-induced (LTI), cold-inducible (KIN), responsive to desiccation (RD), early dehydration-inducible (ERD), and the dehydrin (DHN) genes [44][45][46][47]. The distinctive element of CBFs within the AP2/ERF family is the specific “CBF signature” flanking the AP2 domain [42][48].
CBF1 was the first CBF gene isolated and characterized by Stockinger and colleagues in Arabidopsis thaliana [49]. Subsequently, other important works discovered the CBF family and its role in the model plant [50][51] and then in other 54 genera: 31 dicotyledons, 23 monocotyledons, and 13 woody species [52][53][54][55][56]. In Poaceae, multiple elements of the family were isolated and characterized, either in chilling-sensitive (e.g., rice and maize) or frost-tolerant species (e.g., wheat, barley, and rye) [52][57][58][59]. The CBF genes are characterized by short, mono-exon coding sequences (average length 700 bp) with no introns [52][60][61]. Interestingly, Shi et al. [47] performed a phylogenetic analysis and found that the CBF gene structure is remarkably conserved across various species (monocots/dicots), independently of their degree of frost tolerance. As reported by Campoli et al. and Badawi et al. [62][63], CBF genes are classified into four phylogenetic groups, each with two or more sub-groups. Some elements of the CBF gene family are scattered along the genome, while others, more frequently, are organized in clusters of tandemly duplicated genes on the long arm of homoeologous chromosome group 5 of Triticeae [64][65][66][67]. The cluster of CBF genes has been shown to coincide with a QTL for frost tolerance, namely Frost Resistance 2 (FR-2) in barley (FR-H2), diploid (FR-Am2) and polyploid wheats (FR-A2 and FR-B2), and rye (FR-R2) [64][67][68]. In Triticeae crops, beside FR-2, part of the phenotypic variation for frost tolerance is attributed to another QTL located about 25–30 cM apart from FR-2 on the long arm of homoeologous chromosome group 5: Frost Resistance 1 (FR-1). This locus was identified by Hayes et al. in 1993 and Galiba et al. in 1995 [66][69] in barley and wheat, respectively, and reported to co-segregate with VRN-1, the vernalization requirement gene [64], whose expression leads the plant to become competent for flowering [70].
Thirteen TmCBF were described in Triticum monococcum L.; eleven of them were mapped on FR-Am2, while TmCBF15 and TmCBF18 were mapped on chromosomes 7Am and 6Am, respectively [71]. Vágújfalvi et al. [67] attributed the locus for FT to chromosome 5A, and subsequently Knox and colleagues [72] divided the FR-A2 locus into: proximal (CBF 2, 4, 9, and 17), central (CBF 12, 14, and 15), and distal (CBF 3, 10, 13, and 16).
The genome of hexaploid wheat encodes 65 TaCBFs [73], 27 of which are paralogs with 1–3 homoeologous A, B, and D copies [73]. As reported by The International Wheat Genome Sequencing Consortium (IWGSC) [74], 54 TaCBFs are located on chromosome Group 5: 17 genes on 5A, 19 on 5B, and 18 on 5D chromosomes. Other TaCBFs are located on homoloegous chromosomes 6 (A, B, and D).

3. Role of the ICE-CBF-COR Pathway in Cold Acclimation

In winter cereals, cold acclimation, also known as “hardening”, has the vital function of protecting the crown and young leaves from ice damage [75]. Even after a severe stress episode, if the crown and young leaves survive, the plant maintains the potential to restore from tillering nodes [76]. This peculiarity is linked to the ability of the meristematic tissue to survive thanks to the physiological phenomenon of cold acclimation [77]. Phenolic compounds, sugars, soluble proteins, new enzyme isoforms, proline and organic acids, modification of the fatty acid composition in the phospholipid membrane, and higher levels of antioxidants are all proactive compounds connected to the reduction of frost damage [43][75][78][79].
In winter barley, wheat, and rye, cold acclimation occurs only in the vegetative phase, and it has two different signaling pathways: abscisic acid or ABA-dependent (ABA pathway) and ABA-independent (also known as the ICE-CBF-COR pathway) [80]. Although the ABA and CBF signal transmissions were considered distinct from each other, recent studies suggest a cross-talk between these two pathways [81].
In short-day conditions, the ICE-CBF-COR pathway is promptly activated after a brief exposure to low, non-harmful temperatures [82][83], and the CBF gene has a pivotal role in the coordination of the acclimation processes [84]. In Arabidopsis, a marked increase in CBF transcript levels was observed 15 min after cold exposure, followed by up-regulation of the effector genes about 2 h later [32][85]. On the other hand, in wheat and barley, an increase in CBF transcript levels was observed 4–12 h later after the cold exposure [86][87][88]. The gene induction relies on a temperature threshold dependent on the species and occurs in a 10 °C to 12 °C range in winter barley, wheat, and rye [89][90]. The result of the ICE-CBF-COR pathway cascade is the activation of the effector genes that modify the plant metabolism, conferring frost tolerance [91]. The temperature must be below 10 °C for 4–6 weeks in short-day conditions to complete the adaptive response in Triticeae [92][93]; once the process is completed, crops can withstand freezing at −7/12 °C for barley, −9/18 °C for wheat, and −18/−30 °C for rye [82][94].
Interestingly, no receptors receiving the low temperature signal have been identified so far [78]. The ICE-CBF-COR pathway is activated by an increase in intracellular Ca2+ concentration by either rigidification of the plasma membrane or ligand-activated channels. After calcium influx into the cytosol and its binding by Ca-sensors (such as calmodulins), a signal cascade based on calcium-binding proteins (CBPs) is initiated to target the ICE (inducers of CBF-gene expression) transcription factors that up-regulate the CBF genes [95][96]. ICE transcription factors belong to the MYC family and MYC subfamily of bHLH (basic helix–loop–helix) [97] and are known as positive CBF expression regulators, considered to act upstream of the low-temperature signaling pathway [97][98][99].
In addition, temperature variation is not the only environmental stimulus influencing the expression of the CBFs; also, circadian rhythms and light characteristics (i.e., quality and quantity) have been reported to be involved in cold acclimation [83]. For example, recent studies showed that the expression of some barley HvCBF genes (HvCBF2A, HvCBF4B, HvCBF6, and HvCBF14) is regulated by the circadian rhythm and day length [83][100][101]. In warm conditions, CBF genes show high expression late in the afternoon and continue to decrease early in the night [100]. The peak of expression is 8–12 h after the dawn, either in short- or long-day conditions. However, the amplitude of the peaks is wider in short-day compared to long-day conditions [102]. This peak does not coincide with the coolest period of the day, but it may be functional for the preparation of the cell for the subsequent cold of the night [63]. The circadian clock regulates the expression of several genes. The G-Box-like motifs are necessary for transcriptional regulation by the circadian pseudo-response regulators binding basic helix–loop–helix transcription factors [103]. Other environmental stimuli are the light spectra and intensity; several works have elucidated that the variation of light spectra and light intensity might modulate the expression of CBF genes and also increase frost tolerance [46][104][105][106][107][108].
The vernalization process is controlled by three major genes: VRN-1, VRN-2, and VRN-3 [109][110]. VRN-1 is a flowering promoter that was shown to be an AP1-like MADS-box transcription factor, whose expression leads the plant to the transition from the vegetative to the reproductive phase [111][112]. Moreover, it was also proven to be involved in cold acclimation and frost tolerance [113]. VRN-2 is a dominant flowering repressor down-regulated by vernalization treatment and includes two tandem zinc finger-CCT domain genes (ZCCT1 and ZCCT2) [31][114]. VRN-3, the main integrator of the photoperiod and vernalization signals that lead to the transition of the apical meristem [115], is homologous to the flowering integrator FLOWERING LOCUS T gene in Arabidopsis [116][117]. Due to their diploid nature, WH barleys can be considered a model for vernalization in Triticeae crops [24]. VRN-H2 is expressed in long and neutral day conditions [118]. In autumn, when plants are still in the seedling stages, VRN-H2 is highly expressed and represses the VRN-H3, which is the flowering induction gene [115][119]. The repression of VRN-H3 also limits the expression of VRN-H1 [111][112]. Exposure to cold temperatures activates VRN-H1 and results in the down-regulation of VRN-H2 and, consequently, the release of VRN-H3 from repression [31][109]. After prolonged cold exposure, the expression level of VRN-H1 reaches a threshold necessary to induce the transition phase, up-regulating VRN-H3, and initiating the flowering process [119]. Exposure to long-day conditions mediated by the photoperiod genes PPD-H1 and PPD-H2 is also necessary [120].
The expression of VRN-H1 changes in function of the plant growth habit; as mentioned above, in winter genotypes, the expression of the recessive vrn-h1 allele is induced by prolonged periods of cold [121][122]. The quantity of time under cold and short-day conditions necessary to satisfy the vernalization requirements varies with the geographical origin of the genotype and the environmental condition, changing from 6 to 10 weeks of temperatures in a range between 6 °C and 2 °C under short-day conditions [31][92][93][123]. In spring genotype, the dominant Vrn-h1 allele has a constitutive high expression that rapidly induces the transition [124]. The vernalization in wheat is more complex compared to barley due to the presence of three homoeologous VRN-A1, VRN-B1, and VRN-D1 loci mapped on the long arm of chromosome group 5 [125], with the major effect of VRN-A1 in determining the growth habit [126].
The interaction between VRN-1/FR-1 and FR-2 (CBFs) has also been demonstrated [127]; VRN-H1 can bind promoter regions of the CBF genes, inducing a reduction of their transcription levels; nevertheless, the mechanism is still not fully understood [128][129].
However, a question remains: how does the ICE-CBF-COR pathway confer frost tolerance?

4. FR-2 in Barley—A Synergistic Action of CNV and HvCBF14?

The efforts to identify the molecular mechanisms underlying FR-2 in Triticeae crops were based on integration studies on structural and functional aspects of the locus. Several barley genotypes have been sequenced, and a pan-genome has been assembled [130]. Thanks to this data, FR-H2 was studied in different frost-prone and tolerant genotypes to evaluate the CBFs position in the cluster, the variability in the structure, the CBF coding sequences, and the promoter regions [24][131][132][133][134].
Initially, four HvCBF genes (HvCBF3, HvCBF6, HvCBF9, and HvCBF14) have been selected as candidate genes due to the presence of homologs in other Triticeae already reported to be involved in cold resistance [63][135]. Then, HvCBF14 has emerged as the major candidate for the frost tolerance in barley in several works [46][52][107][128][135][136][137]. Two SNP linked to HvCBF14, associated with frost tolerance, were identified by Fricano and colleagues [135] in an association analysis of a panel of European cultivars, landraces, and H. spontaneum accessions. Later on, a correlation between frost tolerance and the same HvCBF14 gene in spring haplotypes was demonstrated by Guerra et al. [136], who investigated a panel of 403 accessions with exome sequencing-based allele mining.
Structural variation is recognized as a common feature and evolutionary force of genomes, where copy number variations (CNV) and resulting gene dosage effects determine a number of traits/phenotypes in plants [138][139][140][141][142]. One of the first clear associations between CNV and phenotype was reported for the boron-toxicity tolerance in barley [143]. The first indication of the involvement of CNV at the FR-H2 locus and frost tolerance in Triticeae was reported by Knox et al. [144]. Two HvCBF2 paralogs (HvCBF2A and HvCBF2B) and multiple copies of the HvCBF2A-HvCBF4B genomic segment were identified in the frost-tolerant genotypes ‘Dicktoo’ and ‘Nure’. On the other hand, genomic clones of ‘Morex’ and ‘Tremois’ showed only single paralogs of HvCBF4 and HvCBF2. Results on CNV were confirmed by sequencing the same physical region in the tolerant ‘Nure’ [128] and susceptible ‘Morex’ [131] genotypes, in successive, independent experiments. Francia et al. [145] and Rizza et al. [120] confirmed that frost-resistant varieties of barley were characterized by a high number of copies for the HvCBF2 and HvCBF4 genes and maintained two distinct HvCBF2 paralogs (HvCBF2A and HvCBF2B). In summary, the influence of structural variation on determining the FR-2 effect remains a long-standing conundrum and leaves an open question: is the phenotype influenced by the expression of the HvCBF14 gene alone, or are multiple copies of other CBFs involved? Is the number of copies at the HvCBF2A–HvCBF4B segment relevant for the modulation of the HvCBF14 expression level and the resulting phenotype?
The influence of the gene dosage (i.e., the pool of transcripts) of a specific CBF on the expression of other elements of the ICE-CBF-COR pathway was tested/evaluated in two elegant experiments. The overexpression of HvCBF2 in the spring susceptible cultivar ‘Golden Promise’ resulted in higher transcript levels of COR genes; HvCOR14B and HvDHN5, already at warm temperatures, were raised strongly at cold temperatures. Moreover, higher transcription levels of HvCBF12, HvCBF15, and HvCBF16 and greater frost tolerance were observed in overexpressed lines [146]. According to authors, HvCBF2 may activate target genes at warm temperatures, and transcript accumulation for some of them is greatly enhanced by cold temperatures.
The influence of CNV at HvCBF2A-HvCBF4B on the expression levels of HvCBF12, HvCBF14, and HvCBF16 was investigated using the high frost-tolerant variety ‘Admire’ and different descendent genotypes (namely, Missouri barley—MO B lines) by Dhillon and colleagues [101]. MO B lines harboring a higher number of copies of HvCBF2A-HvCBF4B had higher expression levels of all three genes under normal growth conditions.

5. FR-2 in Wheats—CBF Cluster Ploidy

While barley has a diploid genome (2n = 2x = 14, HH) of 5 giga base pairs (Gbp) [147], tetraploid durum wheat (2n = 4x = 28, AABB) has 12 Gbp [148], and hexaploid wheat (2n = 6x = 42, AABBDD) has approximately 17 Gbp [149]. Thereby, FR-2 organization in wheat is more complex compared to barley due to the contribution of one/multiple homoeologous chromosome regions and redundancy caused by the ploidy level [150][151][152]. Wheat exhibits high variability in frost tolerance traits, given that hexaploid wheat genotypes (AABBDD) exhibit greater frost tolerance than diploid (AA) and tetraploid genotypes (AABB) [153][154].
The first works on CBF/FR-2 in wheat were carried out in mapping populations of einkorn diploid wheat (Triticum monococcum L.), which is the ancestor of the A genome in hexaploid wheat and is considered a practical model for the functional genetics of wheat [67][71][72][86][125][155][156]. First expression studies showed the association of CBF genes at the FR-Am2 with the expression of COR genes and frost tolerance [67][86].
TmCBF12, TmCBF14, TmCBF15, and TmCBF16 (central cluster) expression levels were significantly associated with frost tolerance, measured as regrowth capacity after stress. Moreover, a high-density mapping study confirmed that TmCBF12, TmCBF14, and TmCBF15 were the candidates for the observed differences [72].
Thanks to the works carried out on T. monococcum, the number and position of CBF genes in bread wheat were identified in different works. While in barley, a CNV has never been associated with a central cluster at FR-H2 (see above), in diploid and polyploid wheat, a lower copy number of CBF14 in the B genome compared to the A and D genomes was reported [157].
TaCBF14 and TaCBF15 were associated with increased frost tolerance in doubled haploid (DH) mapping populations of ‘Norstar’ × ‘Winter Manitou’ and ‘Norstar’ × ‘Cappelle-Desprez’ (all WH genotypes) [155]. Higher levels of TaCBF14 induced by temperature shift and blue light were reported in winter wheat ‘Cheyenne’ [137].
Recent studies expanded the investigation of ICE-CBF-COR interconnection with other environmental stimuli with high-throughput functional analysis [97][152][158][159][160][161]. Guo et al. [97] carried out RNAseq and qPCR analysis in wheat tissues under different stress conditions, observing the expression of 53 genes belonging to the ICE-CBF-COR signaling cascade that revealed tissue-specific expression patterns of the ICE, CBF, and COR genes under different stress conditions. Six genes related to the ICE-CBF-COR pathway (TaCBF11a, TaCBF16b, TaICE1a, TaICE1d, TaCOR5a, and TaCOR6d.1) were induced by all treatments (drought, heat, drought, and cold). Three genes, two CBFs and one COR (TaCBF1b, TaCBF4a, and TaCOR3b), were induced specifically by cold.
Zheng et al. [161] carried out an isoform sequencing experiment at four leaf stages under frost stress (at −6 °C), and expression levels of TaCBF8a and TaCBF14a decreased, while TaCBF6a, TaCBF9a, TaCBF10a, TaCBF13a, and TaCBF15a expression levels increased. Recently, Wang et al. [158] performed a transcriptome analysis during the vernalization (4 °C) time-course with sampling from one to six weeks. Six CBF genes of the III subgroup were highly expressed exclusively before vernalization (“steady state” at 22 °C), while 10 CBFs, mainly from the IV subgroup, were not expressed before and were highly induced by vernalization, reaching the highest level of expression after three weeks and decreasing after five/six weeks of treatment. Two different homologs of the MYC-like bHLH transcription factor ICE were identified in wheat as TaICE41 and TaICE87 [98], and their overexpression in Arabidopsis enhanced frost tolerance after hardening. The recent availability of the wheat genome allowed us to locate three TaICE1 genes on the long arm of homoeologous chromosome group 3; these genes were shown to be induced by drought and cold treatment [97]. In addition, Wang et al. [158] reported that TaICE41 was expressed at extremely high levels after five weeks of vernalization.

6. FR-2 in Rye—Evidence of ICE1 Involvement in the Tolerance

Compared to other Triticeae crops, rye is uniquely tolerant to biotic and abiotic stresses, showing high yield potential under marginal conditions [162][163][164]. However, it received little attention in terms of breeding efforts and genomic research due to its limited distribution worldwide. Likewise barley and rye have a diploid genome (2n = 2x = 14, RR); however, it has not become a reference crop for genomic analysis in the Triticeae tribe due to its elevated level of allogamy and the fact that the first chromosome-scale assembly of its large 7.9 Gbp genome was released only recently, in 2021 [165], showing 92% of repetitive elements [162][166][167][168][169].
Investigation of rye genome evolution and chromosome synteny [169] revealed, as expected, that the chromosome 5R harboring FR-2 and FR-1 loci is entirely collinear with wheat homoeologous chromosome group 5. Initially, eleven ScCBF genes were isolated in a winter rye genome, and nine of them were mapped on chromosome 5R with a cluster organization (FR-R2) [62]. Subsequently, Jung and Seo [162] identified 12 new CBF genes and five new CBF gene alleles. The genome assembly [165] reported CNV for 4 members of CBF Group IV between tolerant and resistant varieties.
Concerning the structure of the locus, FR-R2 haplotyped variation has been associated with different frost tolerance levels in different rye genotypes [165][170].

7. New Frontiers for CBF Genes? CBF Genes in the Drought Stress Adaptative Response

CBF genes are members of a large protein family of the C-repeat binding factor/Dehydration responsive element-binding 1 (CBF/DREB1), known to be involved in the growth and development processes and responses to different environmental stressors (cold, heat, drought, salt, etc.) [171]. CBF genes could thus have in Triticeae a role in a cross-talk between the cold and drought response pathways, as already reported for Arabidopsis [54][172].
The CBF/DREB1 regulon modifies the plant metabolism in conditions of water deficiency, and their activation might also be triggered by drought conditions in the seedling phase [97][173]. In several drought-responsive genes, such as AtRD29A (responsive to desiccation), HvDHN1–HvDHN11 (dehydrin), or AtCOR6.6, a DRE/CRT motif is present in the promoter regions. When drought conditions occur, the plant reduces its water uptake by closing the stomata, which also reduces its CO2 uptake, which results in a reduction in the photosynthesis and physiological activities. To cope with drought stress, plants activate several morphological and physiological modifications to conserve water and reduce its loss. The molecular response to drought follows a similar pathway to cold acclimation due to the same trigger of water scarcity, which activates both responses. As already summarized, water deficit activates, like low temperature stress, two different signaling pathways: ABA-dependent and ABA-independent [81]. The interaction between CBF genes in hormone-mediated acid abscisic (ABA) pathways has been reported [174][175]. In A. thaliana, the ABA-independent pathway is regulated by AtCBF4, which increases the production of a class of small, highly expressed, and stress-inducible proteins called late embryogenesis abundant (LEA), protecting the cellular membranes and the cytoskeleton from desiccation [172][176]. Interestingly, it has been shown in A. thaliana that ABA-responsive genes contain in the promoter regions both the ABA-response cis-element ABRE/ABF and the CRT/DRE motif [177]. Overall, drought stress in barley and wheat can have a significant negative impact on plant growth, yield, and grain quality; however, plants have evolved mechanisms to cope with water scarcity and to survive in dry environments [178]. Nevertheless, which CBF genes and which pathways are activated have not been determined yet [44][100][171]. In a study of A. thaliana transgenic lines, the overexpression of AtCBF1 and AtCBF3 genes resulted in an increase in drought tolerance [179]. A review of the conservative role of CBF genes throughout the Poaceae family reported rice OsDREB1A localized in the cluster OsDREB1H, syntenic with the FR-2 locus on chromosome 5 of Triticeae involved in chilling tolerance [52]. However, few examples of studies of the role of CBF genes in drought tolerance are available for barley and wheat.
A common phenotypic response observed in transgenic lines overexpressing CBF genes in different crops can be identified as an increased tolerance to frost and/or drought and modified growth and development, as originally reported for Arabidopsis [171][179]. Overexpression of two CBF/DREBs (TaDREB3 and TaCBF5L) in wheat and barley was reported to lead to an increase in drought and frost tolerance in transgenic barley. Moreover, in transgenic wheat, the TaCBF5L gene significantly increased the grain yield under severe drought during flowering [180]. Javadi and colleagues mined available GeneChip microarray data [181] in order to detect key genes involved in drought tolerance in barley and identified hub genes from the AP2 and NAC families that might be among the key TFs that regulate drought-stress response in barley. What is interesting is that HvCBF6 (distal cluster of FR-H2) was included among the hub genes. In rye, the PEG treatment (drought condition simulation) revealed that there is a specific type of response to stress among ScCBF genes; most of them were highly responsive to cold stress, whereas ScCBF2 and ScCBF7b were induced by water deprivation and were almost insensitive to low temperature [162]. Guo and colleagues [97] characterized the expression profile of the ICE-CBF-COR pathway in different wheat tissues under different stress conditions. Authors showed that TaCBF11a, TaCBF16b, TaICE1a, TaICE1d, TaCOR5a, and TaCOR6d.1 were induced by drought, and the induction level was higher in tolerant genotypes [160].
The overlapping of cold/frost and drought conditions is a relatively unexpected new form of combination of abiotic stress, and it usually happens during the late autumn, after sowing, when winter genotypes are in the seedling phase. The drought stress in the seedling phase induces root architecture modification that might act as a constitutive resistance mechanism, useful when the stress re-occurs in other phenological phases [182][183][184]. As observed in numerous studies in the past years, CBF overexpression in the model plant Arabidopsis enhances abiotic stress tolerance but, on the other hand, reduces growth. CBF genes are known to interact with plant hormones [81], and the current model of CBF-GA (gibberellic acid) interplay proposes that overexpression of CBFs, either via cold induction or by transgenic means, stimulates the accumulation of DELLAs. Those growth-repressing proteins act downstream in the GA signaling pathway, leading to stunted growth. As far as the underlying molecular mechanism is concerned, in warm temperatures, DELLAs interact with JAZs to prevent JAZs binding to ICE1, leading to its inactivation. In cold temperatures, ICE1 is modified to gain the function for activation of CBF transcription [185]. Understanding the relationship between CBF genes, GA and DELLA proteins might help to get an overall picture of the role of CBFs in plant physiology. One of the new frontiers that regard CBF genes is to evaluate their contribution in the tillering phase, crucial in the growth and development of wheat and barley, as it directly influences the potential yield and overall productivity of cereal crops [186]. Moreover, in this phase, winter cereals reach the maximum of their stress tolerance [28][82][94]. The main actors in tillering formation are gibberellic and abscisic acids; moreover, the roles of VRN-1 and VRN-2 and the photoperiod response gene PPD-1 have been described [187][188][189]. All these components interact with CBF genes; however, mechanisms of interaction are still not clear.


  1. Pingali, P.L. Green Revolution: Impacts, Limits, and the Path Ahead. Proc. Natl. Acad. Sci. USA 2012, 109, 12302–12308.
  2. World Population Prospects 2022, Population Growth Rate File, Estimates Table United Nations Department of Economic and Social Affairs. 2022. Available online: (accessed on 29 November 2022).
  3. Bailey-Serres, J.; Parker, J.E.; Ainsworth, E.A.; Oldroyd, G.E.D.; Schroeder, J.I. Genetic Strategies for Improving Crop Yields. Nature 2019, 575, 109–118.
  4. Evenson, R.E.; Gollin, D. Assessing the Impact of the Green Revolution, 1960 to 2000. Science 2003, 300, 758–762.
  5. Hedden, P. The Genes of the Green Revolution. Trends Genet. 2003, 19, 5–9.
  6. Wik, M.; Pingali, P.; Broca, S. Global Agricultural Performance: Past Trends and Future Prospects; World Bank: Washington, DC, USA, 2008; p. 40.
  7. Foley, J.A.; Ramankutty, N.; Brauman, K.A.; Cassidy, E.S.; Gerber, J.S.; Johnston, M.; Mueller, N.D.; O’Connell, C.; Ray, D.K.; West, P.C.; et al. Solutions for a Cultivated Planet. Nature 2011, 478, 337–342.
  8. Pingali, P.L. The Green Revolution and Crop Biodiversity. In Biological Extinction; Dasgupta, P., Raven, P., McIvor, A., Eds.; Cambridge University Press: Cambridge, UK, 2019; pp. 175–192. ISBN 978-1-108-66867-5.
  9. Kopittke, P.M.; Menzies, N.W.; Wang, P.; McKenna, B.A.; Lombi, E. Soil and the Intensification of Agriculture for Global Food Security. Environ. Int. 2019, 132, 105078.
  10. Zhu, X.-G.; Long, S.P.; Ort, D.R. Improving Photosynthetic Efficiency for Greater Yield. Annu. Rev. Plant Biol. 2010, 61, 235–261.
  11. Schröter, D.; Cramer, W.; Leemans, R.; Prentice, I.C.; Araújo, M.B.; Arnell, N.W.; Bondeau, A.; Bugmann, H.; Carter, T.R.; Gracia, C.A.; et al. Ecosystem Service Supply and Vulnerability to Global Change in Europe. Science 2005, 310, 1333–1337.
  12. Kole, C.; Muthamilarasan, M.; Henry, R.; Edwards, D.; Sharma, R.; Abberton, M.; Batley, J.; Bentley, A.; Blakeney, M.; Bryant, J.; et al. Application of Genomics-Assisted Breeding for Generation of Climate Resilient Crops: Progress and Prospects. Front. Plant Sci. 2015, 6, 563.
  13. Grassini, P.; Eskridge, K.M.; Cassman, K.G. Distinguishing between Yield Advances and Yield Plateaus in Historical Crop Production Trends. Nat. Commun. 2013, 4, 2918.
  14. Khoury, C.K.; Brush, S.; Costich, D.E.; Curry, H.A.; De Haan, S.; Engels, J.M.M.; Guarino, L.; Hoban, S.; Mercer, K.L.; Miller, A.J.; et al. Crop Genetic Erosion: Understanding and Responding to Loss of Crop Diversity. New Phytol. 2022, 233, 84–118.
  15. Haussmann, B.I.G.; Parzies, H.K.; Presterl, T.; Suciz, Z.; Miedaner, T. Plant Genetic Resources in Crop Improvement. Plant Genet. Resour. Charact. Util. 2004, 2, 3–21.
  16. Corrado, G.; Rao, R. Special Issue: Plant Genetics and Biotechnology in Biodiversity. Diversity 2018, 10, 19.
  17. Zhao, Y.; Tang, L.; Li, Z.; Jin, J.; Luo, J.; Gao, G. Identification and Analysis of Unitary Loss of Long-Established Protein-Coding Genes in Poaceae Shows Evidences for Biased Gene Loss and Putatively Functional Transcription of Relics. BMC Evol. Biol. 2015, 15, 66.
  18. Zenda, T.; Liu, S.; Dong, A.; Duan, H. Advances in Cereal Crop Genomics for Resilience under Climate Change. Life 2021, 11, 502.
  19. Doebley, J.F.; Gaut, B.S.; Smith, B.D. The Molecular Genetics of Crop Domestication. Cell 2006, 127, 1309–1321.
  20. Intergovernmental Panel on Climate Change. Climate Change and Land: IPCC Special Report on Climate Change, Desertification, Land Degradation, Sustainable Land Management, Food Security, and Greenhouse Gas Fluxes in Terrestrial Ecosystems, 1st ed.; Cambridge University Press: Cambridge, UK, 2022; ISBN 978-1-00-915798-8.
  21. Kovak, E.; Blaustein-Rejto, D.; Qaim, M. Genetically Modified Crops Support Climate Change Mitigation. Trends Plant Sci. 2022, 27, 627–629.
  22. Challinor, A.J.; Watson, J.; Lobell, D.B.; Howden, S.M.; Smith, D.R.; Chhetri, N. A Meta-Analysis of Crop Yield under Climate Change and Adaptation. Nat. Clim. Change 2014, 4, 287–291.
  23. Reynolds, M.P.; Quilligan, E.; Aggarwal, P.K.; Bansal, K.C.; Cavalieri, A.J.; Chapman, S.C.; Chapotin, S.M.; Datta, S.K.; Duveiller, E.; Gill, K.S.; et al. An Integrated Approach to Maintaining Cereal Productivity under Climate Change. Glob. Food Secur. 2016, 8, 9–18.
  24. Muehlbauer, G.J.; Feuillet, C. (Eds.) Genetics and Genomics of the Triticeae; Springer US: New York, NY, USA, 2009; ISBN 978-0-387-77488-6.
  25. Wang, J.; Vanga, S.; Saxena, R.; Orsat, V.; Raghavan, V. Effect of Climate Change on the Yield of Cereal Crops: A Review. Climate 2018, 6, 41.
  26. FAO; STAT. License: CC BY-NC-SA 3.0 IGO. Available online: (accessed on 7 October 2022).
  27. Barkworth, M.E.; Von Bothmer, R. Scientific Names in the Triticeae. In Genetics and Genomics of the Triticeae; Muehlbauer, G.J., Feuillet, C., Eds.; Springer US: New York, NY, USA, 2009; pp. 3–30. ISBN 978-0-387-77488-6.
  28. Hyles, J.; Bloomfield, M.T.; Hunt, J.R.; Trethowan, R.M.; Trevaskis, B. Phenology and Related Traits for Wheat Adaptation. Heredity 2020, 125, 417–430.
  29. Schreiber, M.; Himmelbach, A.; Börner, A.; Mascher, M. Genetic Diversity and Relationship between Domesticated Rye and Its Wild Relatives as Revealed through Genotyping-by-sequencing. Evol. Appl. 2019, 12, 66–77.
  30. Bond, D.M.; Dennis, E.S.; Finnegan, E.J. The Low Temperature Response Pathways for Cold Acclimation and Vernalization Are Independent: Low Temperature Response Pathways. Plant Cell Environ. 2011, 34, 1737–1748.
  31. Trevaskis, B.; Hemming, M.N.; Peacock, W.J.; Dennis, E.S. HvVRN2 Responds to Daylength, Whereas HvVRN1 Is Regulated by Vernalization and Developmental Status. Plant Physiol. 2006, 140, 1397–1405.
  32. Thomashow, M.F. Molecular Basis of Plant Cold Acclimation: Insights Gained from Studying the CBF Cold Response Pathway: Figure 1. Plant Physiol. 2010, 154, 571–577.
  33. von Bothmer, R.; Sato, K.; Komatsuda, T.; Yasuda, S.; Fischbeck, G. The Domestication of Cultivated Barley. In Developments in Plant Genetics and Breeding; Elsevier: Amsterdam, The Netherlands, 2003; Volume 7, pp. 9–27. ISBN 978-0-444-50585-9.
  34. von Zitzewitz, J.; Cuesta-Marcos, A.; Condon, F.; Castro, A.J.; Chao, S.; Corey, A.; Filichkin, T.; Fisk, S.P.; Gutierrez, L.; Haggard, K.; et al. The Genetics of Winterhardiness in Barley: Perspectives from Genome-Wide Association Mapping. Plant Genome 2011, 4, 76–91.
  35. Stockinger, E.J. Winter Hardiness and the CBF Genes in the Triticeae. In Plant Cold Hardiness: From the Laboratory to the Field; Gusta, L.V., Wisniewski, M.E., Tanino, K.K., Eds.; CABI: Wallingford, UK, 2009; pp. 119–130. ISBN 978-1-84593-513-9.
  36. Muñoz-Amatriaín, M.; Hernandez, J.; Herb, D.; Baenziger, P.S.; Bochard, A.M.; Capettini, F.; Casas, A.; Cuesta-Marcos, A.; Einfeldt, C.; Fisk, S.; et al. Perspectives on Low Temperature Tolerance and Vernalization Sensitivity in Barley: Prospects for Facultative Growth Habit. Front. Plant Sci. 2020, 11, 585927.
  37. Rosicka-Kaczmarek, J.; Makowski, B.; Nebesny, E.; Tkaczyk, M.; Komisarczyk, A.; Nita, Z. Composition and Thermodynamic Properties of Starches from Facultative Wheat Varieties. Food Hydrocoll. 2016, 54, 66–76.
  38. Deng, P.; Wang, M.; Feng, K.; Cui, L.; Tong, W.; Song, W.; Nie, X. Genome-Wide Characterization of Microsatellites in Triticeae Species: Abundance, Distribution and Evolution. Sci. Rep. 2016, 6, 32224.
  39. Feldman, M.; Levy, A.A. Origin and Evolution of Wheat and Related Triticeae Species. In Alien Introgression in Wheat; Molnár-Láng, M., Ceoloni, C., Doležel, J., Eds.; Springer International Publishing: Cham, Switzerland, 2015; pp. 21–76. ISBN 978-3-319-23493-9.
  40. Kumlehn, J.; Zimmermann, G.; Berger, C.; Marthe, C.; Hensel, G. Triticeae Cereals. In Genetic Modification of Plants; Kempken, F., Jung, C., Eds.; Biotechnology in Agriculture and Forestry; Springer: Berlin/Heidelberg, Germany, 2010; Volume 64, pp. 287–306. ISBN 978-3-642-02390-3.
  41. Park, S.; Lee, C.; Doherty, C.J.; Gilmour, S.J.; Kim, Y.; Thomashow, M.F. Regulation of the Arabidopsis CBF Regulon by a Complex Low-temperature Regulatory Network. Plant J. 2015, 82, 193–207.
  42. Akhtar, M.; Jaiswal, A.; Taj, G.; Jaiswal, J.P.; Qureshi, M.I.; Singh, N.K. DREB1/CBF Transcription Factors: Their Structure, Function and Role in Abiotic Stress Tolerance in Plants. J. Genet. 2012, 91, 385–395.
  43. Heidarvand, L.; Maali Amiri, R. What Happens in Plant Molecular Responses to Cold Stress? Acta Physiol. Plant 2010, 32, 419–431.
  44. Choi, D.-W.; Zhu, B.; Close, T.J. The Barley (Hordeum Vulgare L.) Dehydrin Multigene Family: Sequences, Allele Types, Chromosome Assignments, and Expression Characteristics of 11 Dhn Genes of Cv Dicktoo. Theor. Appl. Genet. 1999, 98, 1234–1247.
  45. Ahmad, M.; Alabd, A.; Gao, Y.; Yu, W.; Jamil, W.; Wang, X.; Wei, J.; Ni, J.; Teng, Y.; Bai, S. Three Stress-Responsive NAC Transcription Factors, Pp-SNACs, Differentially and Synergistically Regulate Abiotic Stress in Pear. Sci. Hortic. 2022, 305, 111393.
  46. Ahres, M.; Gierczik, K.; Boldizsár, Á.; Vítámvás, P.; Galiba, G. Temperature and Light-Quality-Dependent Regulation of Freezing Tolerance in Barley. Plants 2020, 9, 83.
  47. Shi, Y.; Ding, Y.; Yang, S. Molecular Regulation of CBF Signaling in Cold Acclimation. Trends Plant Sci. 2018, 23, 623–637.
  48. Skinner, J.S.; von Zitzewitz, J.; Szűcs, P.; Marquez-Cedillo, L.; Filichkin, T.; Amundsen, K.; Stockinger, E.J.; Thomashow, M.F.; Chen, T.H.H.; Hayes, P.M. Structural, Functional, and Phylogenetic Characterization of a Large CBF Gene Family in Barley. Plant Mol. Biol. 2005, 59, 533–551.
  49. Stockinger, E.J.; Gilmour, S.J.; Thomashow, M.F. Arabidopsis Thaliana CBF1 Encodes an AP2 Domain-Containing Transcriptional Activator That Binds to the C-Repeat/DRE, a Cis-Acting DNA Regulatory Element That Stimulates Transcription in Response to Low Temperature and Water Deficit. Proc. Natl. Acad. Sci. USA 1997, 94, 1035–1040.
  50. Medina, J.; Bargues, M.; Terol, J.; Pérez-Alonso, M.; Salinas, J. The Arabidopsis CBF Gene Family Is Composed of Three Genes Encoding AP2 Domain-Containing Proteins Whose Expression Is Regulated by Low Temperature but Not by Abscisic Acid or Dehydration1. Plant Physiol. 1999, 119, 463–470.
  51. Jaglo-Ottosen, K.R.; Gilmour, S.J.; Zarka, D.G.; Schabenberger, O.; Thomashow, M.F. Arabidopsis CBF1 Overexpression Induces COR Genes and Enhances Freezing Tolerance. Science 1998, 280, 104–106.
  52. Tondelli, A.; Francia, E.; Barabaschi, D.; Pasquariello, M.; Pecchioni, N. Inside the CBF Locus in Poaceae. Plant Sci. 2011, 180, 39–45.
  53. Welling, A.; Palva, E.T. Molecular Control of Cold Acclimation in Trees. Physiol Plant 2006, 127, 167–181.
  54. Li, W.; Chen, Y.; Ye, M.; Lu, H.; Wang, D.; Chen, Q. Evolutionary History of the C-Repeat Binding Factor/Dehydration-Responsive Element-Binding 1 (CBF/DREB1) Protein Family in 43 Plant Species and Characterization of CBF/DREB1 Proteins in Solanum Tuberosum. BMC Evol. Biol. 2020, 20, 142.
  55. Hu, Z.; Ban, Q.; Hao, J.; Zhu, X.; Cheng, Y.; Mao, J.; Lin, M.; Xia, E.; Li, Y. Genome-Wide Characterization of the C-Repeat Binding Factor (CBF) Gene Family Involved in the Response to Abiotic Stresses in Tea Plant (Camellia Sinensis). Front. Plant Sci. 2020, 11, 921.
  56. Cheng, H.; Cai, H.; Fu, H.; An, Z.; Fang, J.; Hu, Y.; Guo, D.; Huang, H. Functional Characterization of Hevea Brasiliensis CRT/DRE Binding Factor 1 Gene Revealed Regulation Potential in the CBF Pathway of Tropical Perennial Tree. PLoS ONE 2015, 10, e0137634.
  57. Qin, X.; Huang, T.; Lu, C.; Dang, P.; Zhang, M.; Guan, X.; Wen, P.; Wang, T.-C.; Chen, Y.; Siddique, K.H.M. Benefits and Limitations of Straw Mulching and Incorporation on Maize Yield, Water Use Efficiency, and Nitrogen Use Efficiency. Agric. Water Manag. 2021, 256, 107128.
  58. Dubouzet, J.G.; Sakuma, Y.; Ito, Y.; Kasuga, M.; Dubouzet, E.G.; Miura, S.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. OsDREB Genes in Rice, Oryza Sativa L., Encode Transcription Activators That Function in Drought-, High-Salt- and Cold-Responsive Gene Expression: DREB Transcription Activators in Rice. Plant J. 2003, 33, 751–763.
  59. Nakano, T.; Suzuki, K.; Fujimura, T.; Shinshi, H. Genome-Wide Analysis of the ERF Gene Family in Arabidopsis and Rice. Plant Physiol. 2006, 140, 411–432.
  60. Navarro, M.; Marque, G.; Ayax, C.; Keller, G.; Borges, J.P.; Marque, C.; Teulières, C. Complementary Regulation of Four Eucalyptus CBF Genes under Various Cold Conditions. J. Exp. Bot. 2009, 60, 2713–2724.
  61. Galiba, G.; Vágújfalvi, A.; Li, C.; Soltész, A.; Dubcovsky, J. Regulatory Genes Involved in the Determination of Frost Tolerance in Temperate Cereals. Plant Sci. 2009, 176, 12–19.
  62. Campoli, C.; Matus-Cádiz, M.A.; Pozniak, C.J.; Cattivelli, L.; Fowler, D.B. Comparative Expression of Cbf Genes in the Triticeae under Different Acclimation Induction Temperatures. Mol. Genet. Genom. 2009, 282, 141–152.
  63. Badawi, M.; Danyluk, J.; Boucho, B.; Houde, M.; Sarhan, F. The CBF Gene Family in Hexaploid Wheat and Its Relationship to the Phylogenetic Complexity of Cereal CBFs. Mol. Genet. Genom. 2007, 277, 533–554.
  64. Francia, E.; Rizza, F.; Cattivelli, L.; Stanca, A.M.; Galiba, G.; Tóth, B.; Hayes, P.M.; Skinner, J.S.; Pecchioni, N. Two Loci on Chromosome 5H Determine Low-Temperature Tolerance in a ‘Nure’ (Winter) × ‘Tremois’ (Spring) Barley Map. Theor. Appl. Genet. 2004, 108, 670–680.
  65. Francia, E.; Barabaschi, D.; Tondelli, A.; Laidò, G.; Rizza, F.; Stanca, A.M.; Busconi, M.; Fogher, C.; Stockinger, E.J.; Pecchioni, N. Fine Mapping of a HvCBF Gene Cluster at the Frost Resistance Locus Fr-H2 in Barley. Theor. Appl. Genet. 2007, 115, 1083–1091.
  66. Hayes, P.M.; Blake, T.; Chen, T.H.H.; Tragoonrung, S.; Chen, F.; Pan, A.; Liu, B. Quantitative Trait Loci on Barley ( Hordeum Vulgare L.) Chromosome 7 Associated with Components of Winterhardiness. Genome 1993, 36, 66–71.
  67. Vágújfalvi, A.; Galiba, G.; Cattivelli, L.; Dubcovsky, J. The Cold-Regulated Transcriptional Activator Cbf3 Is Linked to the Frost-Tolerance Locus Fr-A2 on Wheat Chromosome 5A. Mol. Gen. Genom. 2003, 269, 60–67.
  68. Båga, M.; Bahrani, H.; Larsen, J.; Hackauf, B.; Graf, R.J.; Laroche, A.; Chibbar, R.N. Association Mapping of Autumn-Seeded Rye (Secale Cereale L.) Reveals Genetic Linkages between Genes Controlling Winter Hardiness and Plant Development. Sci. Rep. 2022, 12, 5793.
  69. Galiba, G.; Quarrie, S.A.; Sutka, J.; Morgounov, A.; Snape, J.W. RFLP Mapping of the Vernalization (Vrnl) and Frost Resistance (Frl) Genes on Chromosome 5A of Wheat. Theor. Appl. Genet. 1995, 90, 1174–1179.
  70. Amasino, R. Vernalization, Competence, and the Epigenetic Memory of Winter. Plant Cell 2004, 16, 2553–2559.
  71. Miller, A.K.; Galiba, G.; Dubcovsky, J. A Cluster of 11 CBF Transcription Factors Is Located at the Frost Tolerance Locus Fr-A m 2 in Triticum Monococcum. Mol. Genet. Genom. 2006, 275, 193–203.
  72. Knox, A.K.; Li, C.; Vágújfalvi, A.; Galiba, G.; Stockinger, E.J.; Dubcovsky, J. Identification of Candidate CBF Genes for the Frost Tolerance Locus Fr-A m 2 in Triticum Monococcum. Plant Mol. Biol. 2008, 67, 257–270.
  73. Mohseni, S.; Che, H.; Djillali, Z.; Dumont, E.; Nankeu, J.; Danyluk, J. Wheat CBF Gene Family: Identification of Polymorphisms in the CBF Coding Sequence. Genome 2012, 55, 865–881.
  74. The International Wheat Genome Sequencing Consortium (IWGSC); Appels, R.; Eversole, K.; Stein, N.; Feuillet, C.; Keller, B.; Rogers, J.; Pozniak, C.J.; Choulet, F.; Distelfeld, A.; et al. Shifting the Limits in Wheat Research and Breeding Using a Fully Annotated Reference Genome. Science 2018, 361, eaar7191.
  75. Hüner, N.P.A.; Dahal, K.; Bode, R.; Kurepin, L.V.; Ivanov, A.G. Photosynthetic Acclimation, Vernalization, Crop Productivity and ‘the Grand Design of Photosynthesis’. J. Plant Physiol. 2016, 203, 29–43.
  76. Kosová, K.; Vítámvás, P.; Prášil, I.T. Wheat and Barley Dehydrins under Cold, Drought, and Salinity €“ What Can LEA-II Proteins Tell Us about Plant Stress Response? Front. Plant Sci. 2014, 5, 343.
  77. Hüner, N.; Öquist, G.; Hurry, V.M.; Krol, M.; Falk, S.; Griffith, M. Photosynthesis, Photoinhibition and Low Temperature Acclimation in Cold Tolerant Plants. Photosynth. Res. 1993, 37, 19–39.
  78. Fiust, A.; Rapacz, M. Downregulation of Three Novel Candidate Genes Is Important for Freezing Tolerance of Field and Laboratory Cold Acclimated Barley. J. Plant Physiol. 2020, 244, 153049.
  79. Hüner, N.P.A.; Bode, R.; Dahal, K.; Busch, F.A.; Possmayer, M.; Szyszka, B.; Rosso, D.; Ensminger, I.; Krol, M.; Ivanov, A.G.; et al. Shedding Some Light on Cold Acclimation, Cold Adaptation, and Phenotypic Plasticity. Botany 2013, 91, 127–136.
  80. Shi, Y.; Ding, Y.; Yang, S. Cold Signal Transduction and Its Interplay with Phytohormones During Cold Acclimation. Plant Cell Physiol. 2015, 56, 7–15.
  81. Kashyap, P.; Deswal, R. Phytohormones Regulating the Master Regulators of CBF Dependent Cold Stress Signaling Pathway. In Genetic Enhancement of Crops for Tolerance to Abiotic Stress: Mechanisms and Approaches, Vol. I; Rajpal, V.R., Sehgal, D., Kumar, A., Raina, S.N., Eds.; Sustainable Development and Biodiversity; Springer International Publishing: Cham, Switzerland, 2019; Volume 20, pp. 249–264. ISBN 978-3-319-91955-3.
  82. Galiba, G.; Tóth, B. Cold Stress. In Encyclopedia of Applied Plant Sciences; Elsevier: Amsterdam, The Netherlands, 2017; pp. 1–7. ISBN 978-0-12-394808-3.
  83. Maibam, P.; Nawkar, G.; Park, J.; Sahi, V.; Lee, S.; Kang, C. The Influence of Light Quality, Circadian Rhythm, and Photoperiod on the CBF-Mediated Freezing Tolerance. Int. J. Mol. Sci. 2013, 14, 11527–11543.
  84. Kurepin, L.; Dahal, K.; Savitch, L.; Singh, J.; Bode, R.; Ivanov, A.; Hurry, V.; Hüner, N. Role of CBFs as Integrators of Chloroplast Redox, Phytochrome and Plant Hormone Signaling during Cold Acclimation. Int. J. Mol. Sci. 2013, 14, 12729–12763.
  85. Vaultier, M.-N.; Cantrel, C.; Vergnolle, C.; Justin, A.-M.; Demandre, C.; Benhassaine-Kesri, G.; Çiçek, D.; Zachowski, A.; Ruelland, E. Desaturase Mutants Reveal That Membrane Rigidification Acts as a Cold Perception Mechanism Upstream of the Diacylglycerol Kinase Pathway in Arabidopsis Cells. FEBS Lett. 2006, 580, 4218–4223.
  86. Vágújfalvi, A.; Aprile, A.; Miller, A.; Dubcovsky, J.; Delugu, G.; Galiba, G.; Cattivelli, L. The Expression of Several Cbf Genes at the Fr-A2 Locus Is Linked to Frost Resistance in Wheat. Mol. Genet. Genom. 2005, 274, 506–514.
  87. Xue, G.-P. The DNA-Binding Activity of an AP2 Transcriptional Activator HvCBF2 Involved in Regulation of Low-Temperature Responsive Genes in Barley Is Modulated by Temperature. Plant J. 2003, 33, 373–383.
  88. Jin, Y.; Zhai, S.; Wang, W.; Ding, X.; Guo, Z.; Bai, L.; Wang, S. Identification of Genes from the ICE–CBF–COR Pathway under Cold Stress in Aegilops–Triticum Composite Group and the Evolution Analysis with Those from Triticeae. Physiol. Mol. Biol. Plants 2018, 24, 211–229.
  89. Fowler, D.B. Cold Acclimation Threshold Induction Temperatures in Cereals. Crop Sci. 2008, 48, 1147.
  90. Rizza, F.; Pagani, D.; Gut, M.; Prášil, I.T.; Lago, C.; Tondelli, A.; Orrù, L.; Mazzucotelli, E.; Francia, E.; Badeck, F.-W.; et al. Diversity in the Response to Low Temperature in Representative Barley Genotypes Cultivated in Europe. Crop Sci. 2011, 51, 2759–2779.
  91. Crosatti, C.; Marè, C.; Mazzucotelli, E.; Belloni, S.; Barilli, S.; Bassi, R.; Dubcovskyi, J.; Galiba, G.; Stanca, A.M.; Cattivelli, L. Genetic Analysis of the Expression of the Cold-Regulated Gene Cor14b: A Way toward the Identification of Components of the Cold Response Signal Transduction in Triticeae. Can. J. Bot. 2003, 81, 1162–1167.
  92. Cha, J.-K.; O’Connor, K.; Alahmad, S.; Lee, J.-H.; Dinglasan, E.; Park, H.; Lee, S.-M.; Hirsz, D.; Kwon, S.-W.; Kwon, Y.; et al. Speed Vernalization to Accelerate Generation Advance in Winter Cereal Crops. Mol. Plant 2022, 15, 1300–1309.
  93. Xu, S.; Chong, K. Remembering Winter through Vernalisation. Nat. Plants 2018, 4, 997–1009.
  94. Pecchioni, N.; Kosová, K.; Vítámvás, P.; Prášil, I.T.; Milc, J.A.; Francia, E.; Gulyás, Z.; Kocsy, G.; Galiba, G. Genomics of Low-Temperature Tolerance for an Increased Sustainability of Wheat and Barley Production. In Genomics of Plant Genetic Resources; Tuberosa, R., Graner, A., Frison, E., Eds.; Springer: Dordrecht, The Netherlands, 2014; pp. 149–183. ISBN 978-94-007-7574-9.
  95. Miura, K.; Furumoto, T. Cold Signaling and Cold Response in Plants. Int. J. Mol. Sci. 2013, 14, 5312–5337.
  96. Wang, X.; Wu, D.; Yang, Q.; Zeng, J.; Jin, G.; Chen, Z.-H.; Zhang, G.; Dai, F. Identification of Mild Freezing Shock Response Pathways in Barley Based on Transcriptome Profiling. Front. Plant Sci. 2016, 7.
  97. Guo, J.; Ren, Y.; Tang, Z.; Shi, W.; Zhou, M. Characterization and Expression Profiling of the ICE-CBF-COR Genes in Wheat. PeerJ 2019, 7, e8190.
  98. Badawi, M.; Reddy, Y.V.; Agharbaoui, Z.; Tominaga, Y.; Danyluk, J.; Sarhan, F.; Houde, M. Structure and Functional Analysis of Wheat ICE (Inducer of CBF Expression) Genes. Plant Cell Physiol. 2008, 49, 1237–1249.
  99. Chinnusamy, V.; Ohta, M.; Kanrar, S.; Lee, B.; Hong, X.; Agarwal, M.; Zhu, J.-K. ICE1: A Regulator of Cold-Induced Transcriptome and Freezing Tolerance in Arabidopsis. Genes Dev. 2003, 17, 1043–1054.
  100. Gierczik, K.; Novák, A.; Ahres, M.; Székely, A.; Soltész, A.; Boldizsár, Á.; Gulyás, Z.; Kalapos, B.; Monostori, I.; Kozma-Bognár, L.; et al. Circadian and Light Regulated Expression of CBFs and Their Upstream Signalling Genes in Barley. Int. J. Mol. Sci. 2017, 18, 1828.
  101. Dhillon, T.; Morohashi, K.; Stockinger, E.J. CBF2A–CBF4B Genomic Region Copy Numbers alongside the Circadian Clock Play Key Regulatory Mechanisms Driving Expression of FR-H2 CBFs. Plant Mol. Biol. 2017, 94, 333–347.
  102. Lee, C.-M.; Thomashow, M.F. 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.
  103. Liu, T.L.; Newton, L.; Liu, M.-J.; Shiu, S.-H.; Farré, E.M. A G-Box-Like Motif Is Necessary for Transcriptional Regulation by Circadian Pseudo-Response Regulators in Arabidopsis. Plant Physiol. 2016, 170, 528–539.
  104. Ahres, M.; Pálmai, T.; Kovács, T.; Kovács, L.; Lacek, J.; Vankova, R.; Galiba, G.; Borbély, P. The Effect of White Light Spectrum Modifications by Excess of Blue Light on the Frost Tolerance, Lipid- and Hormone Composition of Barley in the Early Pre-Hardening Phase. Plants 2022, 12, 40.
  105. Ahres, M.; Pálmai, T.; Gierczik, K.; Dobrev, P.; Vanková, R.; Galiba, G. The Impact of Far-Red Light Supplementation on Hormonal Responses to Cold Acclimation in Barley. Biomolecules 2021, 11, 450.
  106. Monostori, I.; Heilmann, M.; Kocsy, G.; Rakszegi, M.; Ahres, M.; Altenbach, S.B.; Szalai, G.; Pál, M.; Toldi, D.; Simon-Sarkadi, L.; et al. LED Lighting—Modification of Growth, Metabolism, Yield and Flour Composition in Wheat by Spectral Quality and Intensity. Front. Plant Sci. 2018, 9, 605.
  107. Novák, A.; Boldizsár, Á.; Gierczik, K.; Vágújfalvi, A.; Ádám, É.; Kozma-Bognár, L.; Galiba, G. Light and Temperature Signalling at the Level of CBF14 Gene Expression in Wheat and Barley. Plant Mol. Biol. Rep. 2017, 35, 399–408.
  108. Kovács, T.; Ahres, M.; Pálmai, T.; Kovács, L.; Uemura, M.; Crosatti, C.; Galiba, G. Decreased R:FR Ratio in Incident White Light Affects the Composition of Barley Leaf Lipidome and Freezing Tolerance in a Temperature-Dependent Manner. Int. J. Mol. Sci. 2020, 21, 7557.
  109. Szùcs, P.; Skinner, J.S.; Karsai, I.; Cuesta-Marcos, A.; Haggard, K.G.; Corey, A.E.; Chen, T.H.H.; Hayes, M.P. Validation of the VRN-H2/VRN-H1 Epistatic Model in Barley Reveals That Intron Length Variation in VRN-H1 May Account for a Continuum of Vernalization Sensitivity. Mol. Genet. Genom. 2007, 277, 249–261.
  110. Cao, Y.; Hu, G.; Zhuang, M.; Yin, J.; Wang, X. Molecular Cloning and Functional Characterization of TaIRI9 Gene in Wheat (Triticum Aestivum L.). Gene 2021, 791, 145694.
  111. Distelfeld, A.; Li, C.; Dubcovsky, J. Regulation of Flowering in Temperate Cereals. Curr. Opin. Plant Biol. 2009, 12, 178–184.
  112. Trevaskis, B.; Hemming, M.N.; Dennis, E.S.; Peacock, W.J. The Molecular Basis of Vernalization-Induced Flowering in Cereals. Trends Plant Sci. 2007, 12, 352–357.
  113. Dhillon, T.; Pearce, S.P.; Stockinger, E.J.; Distelfeld, A.; Li, C.; Knox, A.K.; Vashegyi, I.; Vágújfalvi, A.; Galiba, G.; Dubcovsky, J. Regulation of Freezing Tolerance and Flowering in Temperate Cereals: The VRN-1 Connection. Plant Physiol. 2010, 153, 1846–1858.
  114. Karsai, I.; Szűcs, P.; Mészáros, K.; Filichkina, T.; Hayes, P.M.; Skinner, J.S.; Láng, L.; Bedő, Z. The Vrn-H2 Locus Is a Major Determinant of Flowering Time in a Facultative × Winter Growth Habit Barley (Hordeum Vulgare L.) Mapping Population. Theor. Appl. Genet. 2005, 110, 1458–1466.
  115. Fernández-Calleja, M.; Casas, A.M.; Igartua, E. Major Flowering Time Genes of Barley: Allelic Diversity, Effects, and Comparison with Wheat. Theor. Appl. Genet. 2021, 134, 1867–1897.
  116. Faure, S.; Higgins, J.; Turner, A.; Laurie, D.A. The FLOWERING LOCUS T-Like Gene Family in Barley (Hordeum Vulgare). Genetics 2007, 176, 599–609.
  117. Yan, L.; Fu, D.; Li, C.; Blechl, A.; Tranquilli, G.; Bonafede, M.; Sanchez, A.; Valarik, M.; Yasuda, S.; Dubcovsky, J. The Wheat and Barley Vernalization Gene VRN3 Is an Orthologue of FT. Proc. Natl. Acad. Sci. USA 2006, 103, 19581–19586.
  118. Monteagudo, A.; Igartua, E.; Contreras-Moreira, B.; Gracia, M.P.; Ramos, J.; Karsai, I.; Casas, A.M. Fine-Tuning of the Flowering Time Control in Winter Barley: The Importance of HvOS2 and HvVRN2 in Non-Inductive Conditions. BMC Plant Biol. 2019, 19, 113.
  119. Hemming, M.N.; Fieg, S.; James Peacock, W.; Dennis, E.S.; Trevaskis, B. Regions Associated with Repression of the Barley (Hordeum Vulgare) VERNALIZATION1 Gene Are Not Required for Cold Induction. Mol. Genet. Genom. 2009, 282, 107–117.
  120. Rizza, F.; Karsai, I.; Morcia, C.; Badeck, F.-W.; Terzi, V.; Pagani, D.; Kiss, T.; Stanca, A.M. Association between the Allele Compositions of Major Plant Developmental Genes and Frost Tolerance in Barley (Hordeum Vulgare L.) Germplasm of Different Origin. Mol. Breed. 2016, 36, 156.
  121. Cuesta-Marcos, A.; Szűcs, P.; Close, T.J.; Filichkin, T.; Muehlbauer, G.J.; Smith, K.P.; Hayes, P.M. Genome-Wide SNPs and Re-Sequencing of Growth Habit and Inflorescence Genes in Barley: Implications for Association Mapping in Germplasm Arrays Varying in Size and Structure. BMC Genom. 2010, 11, 707.
  122. Cuesta-Marcos, A.; Muñoz-Amatriaín, M.; Filichkin, T.; Karsai, I.; Trevaskis, B.; Yasuda, S.; Hayes, P.; Sato, K. The Relationships between Development and Low Temperature Tolerance in Barley Near Isogenic Lines Differing for Flowering Behavior. Plant Cell Physiol. 2015, 56, 2312–2324.
  123. Maeda, A.E.; Nakamichi, N. Plant Clock Modifications for Adapting Flowering Time to Local Environments. Plant Physiol. 2022, 190, 952–967.
  124. Shcherban, A.B.; Strygina, K.V.; Salina, E.A. VRN-1 Gene- Associated Prerequisites of Spring Growth Habit in Wild Tetraploid Wheat T. Dicoccoides and the Diploid A Genome Species. BMC Plant Biol. 2015, 15, 94.
  125. Tóth, B.; Galiba, G.; Fehér, E.; Sutka, J.; Snape, J.W. Mapping Genes Affecting Flowering Time and Frost Resistance on Chromosome 5B of Wheat. Theor. Appl. Genet. 2003, 107, 509–514.
  126. Todorovska, E.G.; Kolev, S.; Christov, N.K.; Balint, A.; Kocsy, G.; Vágújfalvi, A.; Galiba, G. The Expression of CBF Genes at Fr-2 Locus Is Associated with the Level of Frost Tolerance in Bulgarian Winter Wheat Cultivars. Biotechnol. Biotechnol. Equip. 2014, 28, 392–401.
  127. Stockinger, E.J.; Skinner, J.S.; Gardner, K.G.; Francia, E.; Pecchioni, N. Expression Levels of Barley Cbf Genes at the Frost Resistance—H2 Locus Are Dependent upon Alleles at Fr-H1 and Fr-H2: Expression Levels of Barley Cbf Genes. Plant J. 2007, 51, 308–321.
  128. Mareri, L.; Milc, J.; Laviano, L.; Buti, M.; Vautrin, S.; Cauet, S.; Mascagni, F.; Natali, L.; Cavallini, A.; Bergès, H.; et al. Influence of CNV on Transcript Levels of HvCBF Genes at Fr-H2 Locus Revealed by Resequencing in Resistant Barley Cv. ‘Nure’ and Expression Analysis. Plant Sci. 2020, 290, 110305.
  129. Deng, W.; Casao, M.C.; Wang, P.; Sato, K.; Hayes, P.M.; Finnegan, E.J.; Trevaskis, B. Direct Links between the Vernalization Response and Other Key Traits of Cereal Crops. Nat. Commun. 2015, 6, 5882.
  130. Jayakodi, M.; Padmarasu, S.; Haberer, G.; Bonthala, V.S.; Gundlach, H.; Monat, C.; Lux, T.; Kamal, N.; Lang, D.; Himmelbach, A.; et al. The Barley Pan-Genome Reveals the Hidden Legacy of Mutation Breeding. Nature 2020, 588, 284–289.
  131. Pasquariello, M.; Barabaschi, D.; Himmelbach, A.; Steuernagel, B.; Ariyadasa, R.; Stein, N.; Gandolfi, F.; Tenedini, E.; Bernardis, I.; Tagliafico, E.; et al. The Barley Frost Resistance-H2 Locus. Funct. Integr. Genom. 2014, 14, 85–100.
  132. Galiba, G.; Stockinger, E.J.; Francia, E.; Milc, J.A.; Kocsy, G.; Pecchioni, N. Freezing Tolerance in the Triticeae. In Translational Genomics for Crop Breeding; Wiley Blackwell: Hoboken, NJ, USA, 2013; Volume 2.
  133. Visioni, A.; Tondelli, A.; Francia, E.; Pswarayi, A.; Malosetti, M.; Russell, J.; Thomas, W.; Waugh, R.; Pecchioni, N.; Romagosa, I.; et al. Genome-Wide Association Mapping of Frost Tolerance in Barley (Hordeum Vulgare L.). BMC Genom. 2013, 14, 424.
  134. Stein, N.; Muehlbauer, G.J. (Eds.) The Barley Genome; Compendium of Plant Genomes; Springer International Publishing: Cham, Switzerland, 2018; ISBN 978-3-319-92527-1.
  135. Fricano, A.; Rizza, F.; Faccioli, P.; Pagani, D.; Pavan, P.; Stella, A.; Rossini, L.; Piffanelli, P.; Cattivelli, L. Genetic Variants of HvCbf14 Are Statistically Associated with Frost Tolerance in a European Germplasm Collection of Hordeum Vulgare. Theor. Appl. Genet. 2009, 119, 1335–1348.
  136. Guerra, D.; Morcia, C.; Badeck, F.; Rizza, F.; Delbono, S.; Francia, E.; Milc, J.A.; Monostori, I.; Galiba, G.; Cattivelli, L.; et al. Extensive Allele Mining Discovers Novel Genetic Diversity in the Loci Controlling Frost Tolerance in Barley. Theor. Appl. Genet. 2022, 135, 553–569.
  137. Novák, A.; Boldizsár, Á.; Ádám, É.; Kozma-Bognár, L.; Majláth, I.; Båga, M.; Tóth, B.; Chibbar, R.; Galiba, G. Light-Quality and Temperature-Dependent CBF14 Gene Expression Modulates Freezing Tolerance in Cereals. EXBOTJ 2016, 67, 1285–1295.
  138. Francia, E.; Pecchioni, N.; Policriti, A.; Scalabrin, S. CNV and Structural Variation in Plants: Prospects of NGS Approaches. In Advances in the Understanding of Biological Sciences Using Next Generation Sequencing (NGS) Approaches; Sablok, G., Kumar, S., Ueno, S., Kuo, J., Varotto, C., Eds.; Springer International Publishing: Cham, Switzerland, 2015; pp. 211–232. ISBN 978-3-319-17156-2.
  139. Cook, D.E.; Lee, T.G.; Guo, X.; Melito, S.; Wang, K.; Bayless, A.M.; Wang, J.; Hughes, T.J.; Willis, D.K.; Clemente, T.E.; et al. Copy Number Variation of Multiple Genes at Rhg1 Mediates Nematode Resistance in Soybean. Science 2012, 338, 1206–1209.
  140. Maron, L.G.; Guimarães, C.T.; Kirst, M.; Albert, P.S.; Birchler, J.A.; Bradbury, P.J.; Buckler, E.S.; Coluccio, A.E.; Danilova, T.V.; Kudrna, D.; et al. Aluminum Tolerance in Maize Is Associated with Higher MATE1 Gene Copy Number. Proc. Natl. Acad. Sci. USA 2013, 110, 5241–5246.
  141. Yin, M.; Zhang, S.; Du, X.; Mateo, R.G.; Guo, W.; Li, A.; Wang, Z.; Wu, S.; Chen, J.; Liu, J.; et al. Genomic Analysis of Medicago Ruthenica Provides Insights into Its Tolerance to Abiotic Stress and Demographic History. Mol. Ecol. Resour. 2021, 21, 1641–1657.
  142. Dolatabadian, A.; Patel, D.A.; Edwards, D.; Batley, J. Copy Number Variation and Disease Resistance in Plants. Theor. Appl. Genet. 2017, 130, 2479–2490.
  143. Sutton, T.; Baumann, U.; Hayes, J.; Collins, N.C.; Shi, B.-J.; Schnurbusch, T.; Hay, A.; Mayo, G.; Pallotta, M.; Tester, M.; et al. Boron-Toxicity Tolerance in Barley Arising from Efflux Transporter Amplification. Science 2007, 318, 1446–1449.
  144. Knox, A.K.; Dhillon, T.; Cheng, H.; Tondelli, A.; Pecchioni, N.; Stockinger, E.J. CBF Gene Copy Number Variation at Frost Resistance-2 Is Associated with Levels of Freezing Tolerance in Temperate-Climate Cereals. Theor. Appl. Genet. 2010, 121, 21–35.
  145. Francia, E.; Morcia, C.; Pasquariello, M.; Mazzamurro, V.; Milc, J.A.; Rizza, F.; Terzi, V.; Pecchioni, N. Copy Number Variation at the HvCBF4–HvCBF2 Genomic Segment Is a Major Component of Frost Resistance in Barley. Plant Mol. Biol. 2016, 92, 161–175.
  146. Jeknić, Z.; Pillman, K.A.; Dhillon, T.; Skinner, J.S.; Veisz, O.; Cuesta-Marcos, A.; Hayes, P.M.; Jacobs, A.K.; Chen, T.H.H.; Stockinger, E.J. 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.
  147. Ogihara, Y.; Takumi, S.; Handa, H. (Eds.) Advances in Wheat Genetics: From Genome to Field; Springer: Tokyo, Japan, 2015; ISBN 978-4-431-55674-9.
  148. Maccaferri, M.; Harris, N.S.; Twardziok, S.O.; Pasam, R.K.; Gundlach, H.; Spannagl, M.; Ormanbekova, D.; Lux, T.; Prade, V.M.; Milner, S.G.; et al. Durum Wheat Genome Highlights Past Domestication Signatures and Future Improvement Targets. Nat. Genet. 2019, 51, 885–895.
  149. Smith, D.B.; Flavell, R.B. Characterisation of the Wheat Genome by Renaturation Kinetics. Chromosoma 1975, 50.
  150. Pearce, S.; Zhu, J.; Boldizsár, Á.; Vágújfalvi, A.; Burke, A.; Garland-Campbell, K.; Galiba, G.; Dubcovsky, J. Large Deletions in the CBF Gene Cluster at the Fr-B2 Locus Are Associated with Reduced Frost Tolerance in Wheat. Theor. Appl. Genet. 2013, 126, 2683–2697.
  151. Bolouri, P.; Haliloğlu, K.; Mohammadi, S.A.; Türkoğlu, A.; İlhan, E.; Niedbała, G.; Szulc, P.; Niazian, M. Identification of Novel QTLs Associated with Frost Tolerance in Winter Wheat (Triticum Aestivum L.). Plants 2023, 12, 1641.
  152. Li, L.; Han, C.; Yang, J.; Tian, Z.; Jiang, R.; Yang, F.; Jiao, K.; Qi, M.; Liu, L.; Zhang, B.; et al. Comprehensive Transcriptome Analysis of Responses during Cold Stress in Wheat (Triticum Aestivum L.). Genes 2023, 14, 844.
  153. Fowler, D.B.; Dvorak, J.; Gusta, L.v. Comparative Cold Hardiness of Several Triticum Species and Secale Cereale L.1. Crop Sci. 1977, 17, 941–943.
  154. Limin, A.E.; Fowler, D.B. Cold Hardiness of Some Relatives of Hexaploid Wheat. Can. J. Bot. 1981, 59, 572–573.
  155. Båga, M.; Chodaparambil, S.V.; Limin, A.E.; Pecar, M.; Fowler, D.B.; Chibbar, R.N. Identification of Quantitative Trait Loci and Associated Candidate Genes for Low-Temperature Tolerance in Cold-Hardy Winter Wheat. Funct. Integr. Genom. 2006, 7, 53–68.
  156. Saripalli, G.; Adhikari, L.; Amos, C.; Kibriya, A.; Ahmed, H.I.; Heuberger, M.; Raupp, J.; Athiyannan, N.; Wicker, T.; Abrouk, M.; et al. Integration of Genetic and Genomics Resources in Einkorn Wheat Enables Precision Mapping of Important Traits. Commun. Biol. 2023, 6, 835.
  157. Dhillon, T.; Stockinger, E.J. Cbf14 Copy Number Variation in the A, B, and D Genomes of Diploid and Polyploid Wheat. Theor. Appl. Genet. 2013, 126, 2777–2789.
  158. Wang, J.; Sun, L.; Zhang, H.; Jiao, B.; Wang, H.; Zhou, S. Transcriptome Analysis during Vernalization in Wheat (Triticum Aestivum L.). BMC Genom. Data 2023, 24, 43.
  159. Pan, Y.; Li, Y.; Liu, Z.; Zou, J.; Li, Q. Computational Genomics Insights into Cold Acclimation in Wheat. Front. Genet. 2022, 13, 1015673.
  160. Singh, K.; Singh, S.P.; Yadav, M.K. Physio-Biochemical Assessment and CBF Genes Expression Analysis in Wheat under Dehydration Condition. Biologia 2022, 77, 1851–1860.
  161. Zheng, X.; Shi, M.; Wang, J.; Yang, N.; Wang, K.; Xi, J.; Wu, C.; Xi, T.; Zheng, J.; Zhang, J. Isoform Sequencing Provides Insight Into Freezing Response of Common Wheat (Triticum Aestivum L.). Front. Genet. 2020, 11, 462.
  162. Jung, W.J.; Seo, Y.W. Identification of Novel C-Repeat Binding Factor (CBF) Genes in Rye (Secale Cereale L.) and Expression Studies. Gene 2019, 684, 82–94.
  163. Alptekin, B.; Langridge, P.; Budak, H. Abiotic Stress miRNomes in the Triticeae. Funct. Integr. Genom. 2017, 17, 145–170.
  164. Mago, R.; Miah, H.; Lawrence, G.J.; Wellings, C.R.; Spielmeyer, W.; Bariana, H.S.; McIntosh, R.A.; Pryor, A.J.; Ellis, J.G. High-Resolution Mapping and Mutation Analysis Separate the Rust Resistance Genes Sr31, Lr26 and Yr9 on the Short Arm of Rye Chromosome 1. Theor. Appl. Genet. 2005, 112, 41–50.
  165. Rabanus-Wallace, M.T.; Hackauf, B.; Mascher, M.; Lux, T.; Wicker, T.; Gundlach, H.; Baez, M.; Houben, A.; Mayer, K.F.X.; Guo, L.; et al. Chromosome-Scale Genome Assembly Provides Insights into Rye Biology, Evolution and Agronomic Potential. Nat. Genet. 2021, 53, 564–573.
  166. Bartoš, J.; Paux, E.; Kofler, R.; Havránková, M.; Kopecký, D.; Suchánková, P.; Šafář, J.; Šimková, H.; Town, C.D.; Lelley, T.; et al. A First Survey of the Rye (Secale Cereale) Genome Composition through BAC End Sequencing of the Short Arm of Chromosome 1R. BMC Plant Biol 2008, 8, 95.
  167. Flavell, R.B.; Bennett, M.D.; Smith, J.B.; Smith, D.B. Genome Size and the Proportion of Repeated Nucleotide Sequence DNA in Plants. Biochem. Genet. 1974, 12, 257–269.
  168. Martis, M.M.; Zhou, R.; Haseneyer, G.; Schmutzer, T.; Vrána, J.; Kubaláková, M.; König, S.; Kugler, K.G.; Scholz, U.; Hackauf, B.; et al. Reticulate Evolution of the Rye Genome. Plant Cell 2013, 25, 3685–3698.
  169. Li, G.; Wang, L.; Yang, J.; He, H.; Jin, H.; Li, X.; Ren, T.; Ren, Z.; Li, F.; Han, X.; et al. A High-Quality Genome Assembly Highlights Rye Genomic Characteristics and Agronomically Important Genes. Nat. Genet. 2021, 53, 574–584.
  170. Li, Y.; Böck, A.; Haseneyer, G.; Korzun, V.; Wilde, P.; Schön, C.-C.; Ankerst, D.P.; Bauer, E. Association Analysis of Frost Tolerance in Rye Using Candidate Genes and Phenotypic Data from Controlled, Semi-Controlled, and Field Phenotyping Platforms. BMC Plant Biol. 2011, 11, 146.
  171. Wu, Y.; Li, X.; Zhang, J.; Zhao, H.; Tan, S.; Xu, W.; Pan, J.; Yang, F.; Pi, E. ERF Subfamily Transcription Factors and Their Function in Plant Responses to Abiotic Stresses. Front. Plant Sci. 2022, 13, 1042084.
  172. Haake, V.; Cook, D.; Riechmann, J.; Pineda, O.; Thomashow, M.F.; Zhang, J.Z. Transcription Factor CBF4 Is a Regulator of Drought Adaptation in Arabidopsis. Plant Physiol. 2002, 130, 639–648.
  173. Hrmova, M.; Hussain, S.S. Plant Transcription Factors Involved in Drought and Associated Stresses. Int. J. Mol. Sci. 2021, 22, 5662.
  174. Muhammad Aslam, M.; Waseem, M.; Jakada, B.H.; Okal, E.J.; Lei, Z.; Saqib, H.S.A.; Yuan, W.; Xu, W.; Zhang, Q. Mechanisms of Abscisic Acid-Mediated Drought Stress Responses in Plants. Int. J. Mol. Sci. 2022, 23, 1084.
  175. Tuteja, N. Abscisic Acid and Abiotic Stress Signaling. Plant Signal. Behav. 2007, 2, 135–138.
  176. Kaur, G.; Asthir, B. Molecular Responses to Drought Stress in Plants. Biol. Plant. 2017, 61, 201–209.
  177. Uno, Y.; Furihata, T.; Abe, H.; Yoshida, R.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Arabidopsis Basic Leucine Zipper Transcription Factors Involved in an Abscisic Acid-Dependent Signal Transduction Pathway under Drought and High-Salinity Conditions. Proc. Natl. Acad. Sci. USA 2000, 97, 11632–11637.
  178. Salehi-Lisar, S.Y.; Bakhshayeshan-Agdam, H. Drought Stress in Plants: Causes, Consequences, and Tolerance. In Drought Stress Tolerance in Plants, Vol 1; Hossain, M.A., Wani, S.H., Bhattacharjee, S., Burritt, D.J., Tran, L.-S.P., Eds.; Springer International Publishing: Cham, Switzerland, 2016; pp. 1–16. ISBN 978-3-319-28897-0.
  179. Xu, F.; Liu, Z.; Xie, H.; Zhu, J.; Zhang, J.; Kraus, J.; Blaschnig, T.; Nehls, R.; Wang, H. Increased Drought Tolerance through the Suppression of ESKMO1 Gene and Overexpression of CBF-Related Genes in Arabidopsis. PLoS ONE 2014, 9, e106509.
  180. Yang, Y.; Al-Baidhani, H.H.J.; Harris, J.; Riboni, M.; Li, Y.; Mazonka, I.; Bazanova, N.; Chirkova, L.; Sarfraz Hussain, S.; Hrmova, M.; et al. DREB/CBF Expression in Wheat and Barley Using the Stress-inducible Promoters of HD-Zip I Genes: Impact on Plant Development, Stress Tolerance and Yield. Plant Biotechnol. J. 2020, 18, 829–844.
  181. Javadi, S.M.; Shobbar, Z.-S.; Ebrahimi, A.; Shahbazi, M. New Insights on Key Genes Involved in Drought Stress Response of Barley: Gene Networks Reconstruction, Hub, and Promoter Analysis. J. Genet. Eng. Biotechnol. 2021, 19, 2.
  182. Sallam, A.; Alqudah, A.M.; Dawood, M.F.A.; Baenziger, P.S.; Börner, A. Drought Stress Tolerance in Wheat and Barley: Advances in Physiology, Breeding and Genetics Research. Int. J. Mol. Sci. 2019, 20, 3137.
  183. Manschadi, A.M.; Hammer, G.L.; Christopher, J.T.; deVoil, P. Genotypic Variation in Seedling Root Architectural Traits and Implications for Drought Adaptation in Wheat (Triticum Aestivum L.). Plant Soil 2008, 303, 115–129.
  184. Canè, M.A.; Maccaferri, M.; Nazemi, G.; Salvi, S.; Francia, R.; Colalongo, C.; Tuberosa, R. Association Mapping for Root Architectural Traits in Durum Wheat Seedlings as Related to Agronomic Performance. Mol. Breed. 2014, 34, 1629–1645.
  185. Zhou, M.Q.; Shen, C.; Wu, L.H.; Tang, K.X.; Lin, J. CBF-Dependent Signaling Pathway: A Key Responder to Low Temperature Stress in Plants. Crit. Rev. Biotechnol. 2011, 31, 186–192.
  186. Ye, L.; Wang, Y.; Long, L.; Luo, H.; Shen, Q.; Broughton, S.; Wu, D.; Shu, X.; Dai, F.; Li, C.; et al. A Trypsin Family Protein Gene Controls Tillering and Leaf Shape in Barley. Plant Physiol. 2019, 181, 701–713.
  187. Hussien, A.; Tavakol, E.; Horner, D.S.; Muñoz-Amatriaín, M.; Muehlbauer, G.J.; Rossini, L. Genetics of Tillering in Rice and Barley. Plant Genome 2014, 7.
  188. Riaz, A.; Alqudah, A.M.; Kanwal, F.; Pillen, K.; Ye, L.; Dai, F.; Zhang, G. Advances in Studies on Physiological and Molecular Regulation of Barley Tillering. J. Integr. Agric. 2022, 22, 1–13.
  189. Shang, Q.; Wang, Y.; Tang, H.; Sui, N.; Zhang, X.; Wang, F. Genetic, Hormonal, and Environmental Control of Tillering in Wheat. Crop J. 2021, 9, 986–991.
Subjects: Plant Sciences
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to : , , , ,
View Times: 87
Revisions: 2 times (View History)
Update Date: 20 Nov 2023