scholarly journals Integrated Transcriptomics and Metabolomics Analysis Reveal Key Metabolism Pathways Contributing to Cold Tolerance in Peanut

2021 ◽  
Vol 12 ◽  
Author(s):  
Xin Wang ◽  
Yue Liu ◽  
Zhongkui Han ◽  
Yuning Chen ◽  
Dongxin Huai ◽  
...  
Keyword(s):  
Low Temperature ◽  
Cold Tolerance ◽  
Gene Networks ◽  
Cold Resistance ◽  
Chilling Stress ◽  
Soluble Sugar ◽  
Growth Yield ◽  
Limiting Factors ◽  
Accumulation Pattern ◽  
Cold Tolerant

Low temperature (non-freezing) is one of the major limiting factors in peanut (Arachis hypogaea L.) growth, yield, and geographic distribution. Due to the complexity of cold-resistance trait in peanut, the molecular mechanism of cold tolerance and related gene networks were largely unknown. In this study, metabolomic analysis of two peanut cultivars subjected to chilling stress obtained a set of cold-responsive metabolites, including several carbohydrates and polyamines. These substances showed a higher accumulation pattern in cold-tolerant variety SLH than cold-susceptible variety ZH12 under cold stress, indicating their importance in protecting peanut from chilling injuries. In addition, 3,620 cold tolerance genes (CTGs) were identified by transcriptome sequencing, and the CTGs were most significantly enriched in the “phenylpropanoid biosynthesis” pathway. Two vital modules and several novel hub genes were obtained by weighted gene co-expression network analysis (WGCNA). Several key genes involved in soluble sugar, polyamine, and G-lignin biosynthetic pathways were substantially higher and/or responded more quickly in SLH (cold tolerant) than ZH12 (cold susceptible) under low temperature, suggesting they might be crucial contributors during the adaptation of peanut to low temperature. These findings will not only provide valuable resources for study of cold resistance in peanut but also lay a foundation for genetic modification of cold regulators to enhance stress tolerance in crops.

scholarly journals The Methylation Patterns and Transcriptional Responses to Chilling Stress at the Seedling Stage in Rice

2019 ◽  
Vol 20 (20) ◽  
pp. 5089 ◽  
Author(s):  
Hui Guo ◽  
Tingkai Wu ◽  
Shuxing Li ◽  
Qiang He ◽  
Zhanlie Yang ◽  
...  
Keyword(s):  
Gene Expression ◽  
Low Temperature ◽  
Cold Stress ◽  
Cold Tolerance ◽  
Temperature Stress ◽  
Chilling Stress ◽  
Low Temperature Stress ◽  
Expression Level ◽  
Altered Expression ◽  
Cold Tolerant

Chilling stress is considered the major abiotic stress affecting the growth, development, and yield of rice. To understand the transcriptomic responses and methylation regulation of rice in response to chilling stress, we analyzed a cold-tolerant variety of rice (Oryza sativa L. cv. P427). The physiological properties, transcriptome, and methylation of cold-tolerant P427 seedlings under low-temperature stress (2–3 °C) were investigated. We found that P427 exhibited enhanced tolerance to low temperature, likely via increasing antioxidant enzyme activity and promoting the accumulation of abscisic acid (ABA). The Methylated DNA Immunoprecipitation Sequencing (MeDIP-seq) data showed that the number of methylation-altered genes was highest in P427 (5496) and slightly lower in Nipponbare (Nip) and 9311 (4528 and 3341, respectively), and only 2.7% (292) of methylation genes were detected as common differentially methylated genes (DMGs) related to cold tolerance in the three varieties. Transcriptome analyses revealed that 1654 genes had specifically altered expression in P427 under cold stress. These genes mainly belonged to transcription factor families, such as Myeloblastosis (MYB), APETALA2/ethylene-responsive element binding proteins (AP2-EREBP), NAM-ATAF-CUC (NAC) and WRKY. Fifty-one genes showed simultaneous methylation and expression level changes. Quantitative RT-PCR (qRT-PCR) results showed that genes involved in the ICE (inducer of CBF expression)-CBF (C-repeat binding factor)—COR (cold-regulated) pathway were highly expressed under cold stress, including the WRKY genes. The homologous gene Os03g0610900 of the open stomatal 1 (OST1) in rice was obtained by evolutionary tree analysis. Methylation in Os03g0610900 gene promoter region decreased, and the expression level of Os03g0610900 increased, suggesting that cold stress may lead to demethylation and increased gene expression of Os03g0610900. The ICE-CBF-COR pathway plays a vital role in the cold tolerance of the rice cultivar P427. Overall, this study demonstrates the differences in methylation and gene expression levels of P427 in response to low-temperature stress, providing a foundation for further investigations of the relationship between environmental stress, DNA methylation, and gene expression in rice.

scholarly journals MaMAPK3-MaICE1-MaPOD P7 pathway, a positive regulator of cold tolerance in banana

2021 ◽  
Vol 21 (1) ◽  
Author(s):  
Jie Gao ◽  
Tongxin Dou ◽  
Weidi He ◽  
Ou Sheng ◽  
Fangcheng Bi ◽  
...  
Keyword(s):  
Transgenic Plants ◽  
Cold Tolerance ◽  
Molecular Breeding ◽  
Cold Resistance ◽  
Oxidoreductase Activity ◽  
Tropical Fruit ◽  
Over Expression ◽  
Cavendish Banana ◽  
Cold Tolerant ◽  
Necrotic Symptoms

Abstract Background Banana is a tropical fruit with a high economic impact worldwide. Cold stress greatly affects the development and production of banana. Results In the present study, we investigated the functions of MaMAPK3 and MaICE1 involved in cold tolerance of banana. The effect of RNAi of MaMAPK3 on Dajiao (Musa spp. ‘Dajiao’; ABB Group) cold tolerance was evaluated. The leaves of the MaMAPK3 RNAi transgenic plants showed wilting and severe necrotic symptoms, while the wide-type (WT) plants remained normal after cold exposure. RNAi of MaMAPK3 significantly changed the expressions of the cold-responsive genes, and the oxidoreductase activity was significantly changed in WT plants, while no changes in transgenic plants were observed. MaICE1 interacted with MaMAPK3, and the expression level of MaICE1 was significantly decreased in MaMAPK3 RNAi transgenic plants. Over-expression of MaICE1 in Cavendish banana (Musa spp. AAA group) indicated that the cold resistance of transgenic plants was superior to that of the WT plants. The POD P7 gene was significantly up-regulated in MaICE1-overexpressing transgenic plants compared with WT plants, and the POD P7 was proved to interact with MaICE1. Conclusions Taken together, our work provided new and solid evidence that MaMAPK3-MaICE1-MaPOD P7 pathway positively improved the cold tolerance in monocotyledon banana, shedding light on molecular breeding for the cold-tolerant banana or other agricultural species.

scholarly journals Comparative Transcriptome Analysis Reveals Potential Gene Modules Associated with Cold Tolerance in Sugarcane (Saccharum officinarum L.)

2021 ◽  
Author(s):  
Xing Huang ◽  
Yongsheng Liang ◽  
Baoqing Zhang ◽  
Xiupeng Song ◽  
Yangrui Li ◽  
...  
Keyword(s):  
Cold Stress ◽  
Cold Tolerance ◽  
Cold Resistance ◽  
Soluble Sugar ◽  
Resistance Mechanism ◽  
Saccharum Officinarum ◽  
Calcium Signal ◽  
Protein Kinase Activity ◽  
Comparative Transcriptome ◽  
Climate Conditions

AbstractSugarcane is an important crop worldwide, and most sugar is derived directly from sugarcane. Due to its thermophilic nature, the yield of sugarcane is largely influenced by extreme climate conditions, especially cold stress. Therefore, the development of sugarcane with improved cold tolerance is an important goal. However, little is known about the multiple mechanisms underlying cold acclimation at the bud stage in sugarcane. In this study, we emphasized that sensitivity to cold stress was higher for the sugarcane variety ROC22 than for GT42, as determined by physical signs, including bud growth capacity, relative conductivity, malonaldehyde contents, and soluble sugar contents. To understand the factors contributing to the difference in cold tolerance between ROC22 and GT42, comparative transcriptome analyses were performed. We found that genes involved in the regulation of the stability of the membrane system were the relative determinants of difference in cold tolerance. Additionally, genes related to protein kinase activity, starch metabolism, and calcium signal transduction were associated with cold tolerance. Finally, 25 candidate genes, including 23 variety-specific and 2 common genes, and 7 transcription factors were screened out for understanding the possible cold resistance mechanism. The findings of this study provide candidate gene resources for cold resistance and will improve our understanding of the regulation of cold tolerance at the bud stage in sugarcane.

scholarly journals Identification of cold stress responsive microRNAs in cold tolerant and susceptible Hemerocallis fulva by high throughput sequencing

2020 ◽  
Author(s):  
Changbing Huang ◽  
Chun Jiang ◽  
limin Jin ◽  
Huanchao Zhang
Keyword(s):  
Low Temperature ◽  
Cold Stress ◽  
Cold Tolerance ◽  
Temperature Stress ◽  
Stress Responses ◽  
Target Genes ◽  
Low Temperature Stress ◽  
Differentially Expressed ◽  
Differentially Expressed Mirnas ◽  
Cold Tolerant

Abstract Background:Hemerocallis fulva is a perennial herb belonging to Hemerocallis of Hemerocallis. Because of the large and bright colors, it is often used as a garden ornamental plant. But most varieties of H. fulva on the market will wither in winter, which will affect their beauty. It is very important to study the effect of low temperature stress on the physiological indexes of H. fulva and understand the cold tolerance of different H. fulva. MiRNA is a kind of endogenous non coding small molecular RNA with length of 21-24nt. It mainly inhibits protein translation by cutting target genes, and plays an important role in the development of organisms, gene expression and biological stress. Low temperature is the main abiotic stress affecting the production of H. fulva in China, which hinders the growth and development of plants. A comprehensive understanding of the expression pattern of microRNA in H. fulva under low temperature stress can improve our understanding of microRNA mediated stress response. Although there are many studies on miRNAs of various plants under cold stress at home and abroad, there are few studies on miRNAs related to cold stress of H. fulva. It is of great significance to explore the cold stress resistant gene resources of H. fulva, especially the identification and functional research of miRNA closely related to cold stress, for the breeding of excellent H. fulva.Results A total of 5619 cold-responsive miRNAs, 315 putative novel and 5 304 conserved miRNAs, were identified from the leaves and roots of two different varieties ‘Jinyan’ (cold-tolerant) and ‘Lucretius ’ (cold-sensitive), which were stressed under -4 oC for 24 h. Twelve conserved and three novel miRNAs (novel-miR10, novel-miR19 and novel-miR48) were differentially expressed in leaves of ‘Jinyan’ under cold stress. Novel-miR19, novel-miR29 and novel-miR30 were up-regulated in roots of ‘Jinyan’ under cold stress. Thirteen and two conserved miRNAs were deferentially expressed in leaves and roots of ‘Lucretius’ after cold stress. The deferentially expressed miRNAs between two cultivars under cold stress include novel miRNAs and the members of the miR156, miR166 and miR319 families. A total of 6 598 target genes for 6 516 known miRNAs and 82 novel miRNAs were predicted by bioinformatic analysis, mainly involved in metabolic processes and stress responses. Ten differentially expressed miRNAs and predicted target genes were confirmed by quantitative reverse transcription PCR(q-PCR), and the expressional changes of target genes were negatively correlated to differentially expressed miRNAs. Our data indicated that some candidate miRNAs (e.g., miR156a-3-p, miR319a, and novel-miR19) may play important roles in plant response to cold stress.Conclusions Our study indicates that some putative target genes and miRNA mediated metabolic processes and stress responses are significant to cold tolerance in H. fulva.

scholarly journals Comparative transcriptome analysis of the cold resistance of the sterile rice line 33S

PLoS ONE ◽  
2022 ◽  
Vol 17 (1) ◽  
pp. e0261822
Author(s):  
Hongjun Xie ◽  
Mingdong Zhu ◽  
Yaying Yu ◽  
Xiaoshan Zeng ◽  
Guohua Tang ◽  
...  
Keyword(s):  
Low Temperature ◽  
Cold Resistance ◽  
Temperature Response ◽  
Enrichment Analysis ◽  
Abiotic Factor ◽  
Comparative Transcriptome ◽  
Important Species ◽  
Expression Of Genes ◽  
Nutrient Reserve ◽  
Cold Tolerant

Rice (Oryza sativa L.) is one of the most important species for food production worldwide. Low temperature is a major abiotic factor that affects rice germination and reproduction. Here, the underlying regulatory mechanism in seedlings of a TGMS variety (33S) and a cold-sensitive variety (Nipponbare) was investigated by comparative transcriptome. There were 795 differentially expressed genes (DEGs) identified only in cold-treated 33S, suggesting that 33S had a unique cold-resistance system. Functional and enrichment analysis of these DEGs revealed that, in 33S, several metabolic pathways, such as photosynthesis, amino acid metabolism, secondary metabolite biosynthesis, were significantly repressed. Moreover, pathways related to growth and development, including starch and sucrose metabolism, and DNA biosynthesis and damage response/repair, were significantly enhanced. The expression of genes related to nutrient reserve activity were significantly up-regulated in 33S. Finally, three NAC and several ERF transcription factors were predicted to be important in this transcriptional reprogramming. This present work provides valuable information for future investigations of low-temperature response mechanisms and genetic improvement of cold-tolerant rice seedlings.

scholarly journals An R2R3-MYB Transcription Factor RmMYB108 Responds to Chilling Stress of Rosa multiflora and Conferred Cold Tolerance of Arabidopsis

2021 ◽  
Vol 12 ◽  
Author(s):  
Jie Dong ◽  
Lei Cao ◽  
Xiaoying Zhang ◽  
Wuhua Zhang ◽  
Tao Yang ◽  
...  
Keyword(s):  
Low Temperature ◽  
Transgenic Plants ◽  
Plant Growth ◽  
Cold Tolerance ◽  
Temperature Stress ◽  
Chilling Stress ◽  
Low Temperature Stress ◽  
Myb Transcription Factor ◽  
Rosa Multiflora ◽  
R2r3 Myb

A sudden cooling in the early spring or late autumn negatively impacts the plant growth and development. Although a number of studies have characterized the role of the transcription factors (TFs) of plant R2R3-myeloblastosis (R2R3-MYB) in response to biotic and abiotic stress, plant growth, and primary and specific metabolisms, much less is known about their role in Rosa multiflora under chilling stress. In the present study, RmMYB108, which encodes a nuclear-localized R2R3-MYB TF with a self-activation activity, was identified based on the earlier published RNA-seq data of R. multiflora plants exposed to short-term low-temperature stress and also on the results of prediction of the gene function referring Arabidopsis. The RmMYB108 gene was induced by stress due to chilling, salt, and drought and was expressed in higher levels in the roots than in the leaves. The heterologous expression of RmMYB108 in Arabidopsis thaliana significantly enhanced the tolerance of transgenic plants to freezing, water deficit, and high salinity, enabling higher survival and growth rates, earlier flowering and silique formation, and better seed quantity and quality compared with the wild-type (WT) plants. When exposed to a continuous low-temperature stress at 4°C, transgenic Arabidopsis lines–overexpressing RmMYB108 showed higher activities of superoxide dismutase and peroxidase, lower relative conductivity, and lower malondialdehyde content than the WT. Moreover, the initial fluorescence (Fo) and maximum photosynthetic efficiency of photosystem II (Fv/Fm) changed more dramatically in the WT than in transgenic plants. Furthermore, the expression levels of cold-related genes involved in the ICE1 (Inducer of CBF expression 1)-CBFs (C-repeat binding factors)-CORs (Cold regulated genes) cascade were higher in the overexpression lines than in the WT. These results suggest that RmMYB108 was positively involved in the tolerance responses when R. multiflora was exposed to challenges against cold, freeze, salt, or drought and improved the cold tolerance of transgenic Arabidopsis by reducing plant damage and promoting plant growth.

scholarly journals Contribution of Mitochondrial Structure and Respiratory Metabolism to The Cold-Resistance of Alfalfa Seedling Root

2020 ◽  
Author(s):  
Meijun Liu ◽  
Wenjing Zhao ◽  
Haoyang Zhang ◽  
Yuxiang Wang ◽  
Xiaoqing Sui
Keyword(s):  
Low Temperature ◽  
Respiratory Rate ◽  
Cold Tolerance ◽  
Complex I ◽  
Cold Resistance ◽  
Respiratory Metabolism ◽  
Complex Ii ◽  
Seedling Root ◽  
Mitochondrial Structure ◽  
Fall Dormancy

Abstract Background: Fall dormancy of alfalfa is significantly associated with its cold tolerance, while root, the main body of alfalfa for overwintering, is critical for the cold resistance of alfalfa. The effect of low temperature on mitochondrial ultrastructure and respiratory metabolism of alfalfa seedling root with different fall dormancy was examined, to study the root cold resistance mechanism by which fall dormancy affects alfalfa cold tolerance. Results: Low temperature induced mitochondrial swelling, and the decline of ATP and accumulation of H 2 O 2 in alfalfa seedling root. Both the Cytochrome pathway (CP) and Alternative pathway (AP) respiratory rate were restrained and mETC complex I, II, III and IV activities were inhibited directly by low temperature in both kinds of alfalfa seedling root, while the decline of mETC complex II and III activities were more serious in Gannong No. 5. These results indicated that the damage of mitochondrial structure and the inhibition of mETC complex I , II, III and IV activities directly by low temperature declined the ATP synthesis and aggravated the ROS accumulation, which inhibit the growth of alfalfa seedling root. Moreover, the lower damage on mitochondrial structure and mETC complex II, III activities and higher the percent of AP to total respiratory rate lead to the lower ATP lack and H 2 O 2 accumulation, which contributed to the root growth of Xinmu No.4 seedling. Conclusions: Low sensitivity of mitochondrial structural stability and mETC complex II, III and Alternative respiration to low temperature contributed to the root cold resistance of alfalfa with low fall dormancy grade.

scholarly journals NILs of Cold Tolerant Japonica Cultivar Exhibited New QTLs for Mineral Elements in Rice

2021 ◽  
Vol 12 ◽  
Author(s):  
Muhammad Kazim Ali ◽  
Zheng-Hai Sun ◽  
Xiao-Meng Yang ◽  
Xiao-Ying Pu ◽  
Cheng-Li Duan ◽  
...  
Keyword(s):  
Chromosome Number ◽  
Cold Tolerance ◽  
Morphological Analysis ◽  
Chilling Stress ◽  
Mineral Elements ◽  
Leaf Length ◽  
P Element ◽  
Booting Stage ◽  
Cold Tolerant ◽  
Selection Of

Chilling stress at booting stage can cause floret deterioration and sterility by limiting the supply of food chain and the accumulation of essential mineral elements resulting in reduction of yield and grain quality attributes in rice. Genomic selection of chilling tolerant rice with reference to the accumulation of mineral elements will have great potential to cope with malnutrition and food security in times of climate change. Therefore, a study was conducted to explore the genomic determinants of cold tolerance and mineral elements content in near-isogenic lines (NILs) of japonica rice subjected to chilling stress at flowering stage. Detailed morphological analysis followed by quantitative analysis of 17 mineral elements revealed that the content of phosphorus (P, 3,253 mg/kg) and potassium (K, 2,485 mg/kg) were highest while strontium (Sr, 0.26 mg/kg) and boron (B, 0.34 mg/kg) were lowest among the mineral elements. The correlation analysis revealed extremely positive correlation of phosphorus (P) and copper (Cu) with most of the cold tolerance traits. Among all the effective ear and the second leaf length correlation was significant with half of the mineral elements. As a result of comparative analysis, some QTLs (qBRCC-1, qBRCIC-2, qBRZC-6, qBRCHC-6, qBRMC-6, qBRCIC-6a, qBRCIC-6b, qBRCHC-6, and qBRMC-6) identified for calcium (Ca), zinc (Zn), chromium (Cr) and magnesium (Mg) on chromosome number 1, 2, and 6 while, a novel QTL (qBCPC-1) was identified on chromosome number 1 for P element only. These findings provided bases for the identification of candidate genes involved in mineral accumulation and cold tolerance in rice at booting stage.

scholarly journals Tetraploidy  enhances the cold-resistance in yellow kiwifruit (Actinidia chinensis)

2020 ◽  
Author(s):  
Yipei Li ◽  
Xiaozhen Liu ◽  
Zhou Wei ◽  
Zhimin Zhang ◽  
Wen Bian ◽  
...  
Keyword(s):  
Survival Rate ◽  
Low Temperature ◽  
Cold Tolerance ◽  
Regulatory Networks ◽  
Temperature Tolerance ◽  
Temperature Treatment ◽  
Actinidia Chinensis ◽  
Low Temperature Tolerance ◽  
Low Temperature Treatment ◽  
Cold Tolerant

Abstract Yellow kiwifruit ( Actinidia chinensis ) is highly susceptible to severe weather, such as low temperature and frost, which may affect the production in the coming year. And the cold-resistant mechanism of kiwifruit associated with gene regulation is poorly investigated. To botain cold-resistant germplam, to provide insight into the causes of differences in low temperature tolerance due to ploidy and to better understand cold-adaptive mechanisms in tetraploid kiwifruit, the diploid yellow kiwifruit ‘SWFU03’ and its tetraploid plantlets were subjected to cold-tolerant screening with L-hydroxyproline (L-Hyp) and low temperature, the selected ones were then analyzed by transcriptome data and confirmed by RT-qPCR. The results showed that the survival rate of tetraploid plants was 62.22% when treated with 8 mmol/L L-Hyp for 30 days, while all the diploid ones died. After treated with 0°C for 12 h, then at room temperature for seven days, the survival rate of tetraploid plantlets was 42.22%, while all diploidy died. Hence, cold tolerance of the tetraploid plantlets was stronger than that of the diploid genotypes. Using these two screening systems, 126 cold-resistant tetraploid tissue culture plantlets were obtained. A total of 1630 differentially expressed genes (DEGs) were identified, of which 619 were up-regulated and 1011 were down-regulated in the low temperature treatment goup. The DEGs enriched in the cold-tolerance related pathways mainly included plant hormone signal transduction, and starch and sucrose metabolism pathway. RT-qPCR analysis confirmed the expression levels of eight up-regulated genes in these pathways in the cold-resistant mutants. In conclusion, this study has identified cold-resistant yellow kiwifruit plantlets and cold-tolerance related genes. Moreover, the dataset got in this study advances our knowledge of the cold-adaptive genes in the regulatory networks and leads to understand the cold tolerance mechanisms in the tetraploid yellow kiwifruit.

scholarly journals Low Temperature Effect on Different Varieties of Corchorus capsularis and Corchorus olitorius at Seedling Stage

Agronomy ◽  
2021 ◽  
Vol 11 (12) ◽  
pp. 2547
Author(s):  
Susmita Dey ◽  
Ashok Biswas ◽  
Siqi Huang ◽  
Defang Li ◽  
Liangliang Liu ◽  
...  
Keyword(s):  
Low Temperature ◽  
Cold Tolerance ◽  
Defense Mechanism ◽  
Soluble Sugar ◽  
Natural Fibers ◽  
Hierarchical Cluster ◽  
Carotenoid Content ◽  
Enzymatic Antioxidants ◽  
Total Soluble Sugar ◽  
Group I

To address the demand for natural fibers, developing new varieties that are resistant to abiotic stress is necessary. The present study was designed to investigate the physiological and biochemical traits of three varieties of C. capularis (Y49, Y38, and Y1) and four varieties C. olitorius (T8, W57, M33, M18) under low temperature to identify the cold-tolerant varieties and elucidate the mechanisms involved in enhancing cold tolerance. Research findings revealed that the varieties Y49 and M33 exhibited the highest chlorophyll and carotenoid content. Biochemical profiles revealed that varieties Y49 and M33 were found to be able to withstand low-temperature stress by accumulating different enzymatic and non-enzymatic antioxidants, such as superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), ascorbate peroxidase (APx), glutathione (GSH), and phenolics, which participated in reducing the content of malondialdehyde (MDA) and hydrogen peroxide (H2O2) caused by low temperature. Osmolytes compounds, such as total soluble sugar, significantly increased in Y49 and M33; and proline content decreased in all varieties except Y49 and M33 after low-temperature exposure. The rise in these osmolytes molecules can be a defense mechanism for the jute’s osmotic readjustment to reduce the oxidative damage induced by low temperature. Furthermore, PCA and hierarchical cluster analysis distinguished the seven varieties into three separate groups. Results confirmed that group I (Y49 and M33 varieties) were low-temperature tolerant, group II (M18, W57) were intermediate, whereas III groups (Y38, T8, and Y1) were low temperature susceptible. PCA also explained 85.72% of the variance of raw data and clearly distinguished three groups that are similar to the cluster heat map. The study thus confirmed the tolerance of selected varieties that might be an efficient adaptation strategy and utilized them for establishing breeding programs for cold tolerance.

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