DNA methylation affects freezing tolerance in winter rapeseed by mediating the expression of genes related to JA and CK pathways

Winter rapeseed is the largest source of edible oil in China and is especially sensitive to low temperature, which causes tremendous agricultural yield reduction and economic losses. It is still unclear how DNA methylation regulates the formation of freezing tolerance in winter rapeseed under freezi...

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Published inFrontiers in genetics Vol. 13; p. 968494
Main Authors Wei, Jiaping, Shen, Yingzi, Dong, Xiaoyun, Zhu, Yajing, Cui, Junmei, Li, Hui, Zheng, Guoqiang, Tian, Haiyan, Wang, Ying, Liu, Zigang
Format Journal Article
LanguageEnglish
Published Frontiers Media S.A 17.08.2022
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Abstract Winter rapeseed is the largest source of edible oil in China and is especially sensitive to low temperature, which causes tremendous agricultural yield reduction and economic losses. It is still unclear how DNA methylation regulates the formation of freezing tolerance in winter rapeseed under freezing stress. Therefore, in this study, the whole-genome DNA methylation map and transcriptome expression profiles of freezing-resistant cultivar NTS57 (NS) under freezing stress were obtained. The genome-wide methylation assay exhibited lower levels of methylation in gene-rich regions. DNA methylation was identified in three genomic sequence contexts including CG, CHG and CHH, of which CG contexts exhibited the highest methylation levels (66.8%), followed by CHG (28.6%) and CHH (9.5%). Higher levels of the methylation were found in upstream 2 k and downstream 2 k of gene regions, whereas lowest levels were in the gene body regions. In addition, 331, 437, and 1720 unique differentially methylated genes (DMGs) were identified in three genomic sequence contexts in 17NS under freezing stress compared to the control. Function enrichment analysis suggested that most of enriched DMGs were involved in plant hormones signal transduction, phenylpropanoid biosynthesis and protein processing pathways. Changes of genes expression in signal transduction pathways for cytokinin (CK) and jasmonic acid (JA) implied their involvement in freezing stress responses. Collectively, these results suggested a critical role of DNA methylation in their transcriptional regulation in winter rapeseed under freezing stress.
AbstractList Winter rapeseed is the largest source of edible oil in China and is especially sensitive to low temperature, which causes tremendous agricultural yield reduction and economic losses. It is still unclear how DNA methylation regulates the formation of freezing tolerance in winter rapeseed under freezing stress. Therefore, in this study, the whole-genome DNA methylation map and transcriptome expression profiles of freezing-resistant cultivar NTS57 (NS) under freezing stress were obtained. The genome-wide methylation assay exhibited lower levels of methylation in gene-rich regions. DNA methylation was identified in three genomic sequence contexts including CG, CHG and CHH, of which CG contexts exhibited the highest methylation levels (66.8%), followed by CHG (28.6%) and CHH (9.5%). Higher levels of the methylation were found in upstream 2 k and downstream 2 k of gene regions, whereas lowest levels were in the gene body regions. In addition, 331, 437, and 1720 unique differentially methylated genes (DMGs) were identified in three genomic sequence contexts in 17NS under freezing stress compared to the control. Function enrichment analysis suggested that most of enriched DMGs were involved in plant hormones signal transduction, phenylpropanoid biosynthesis and protein processing pathways. Changes of genes expression in signal transduction pathways for cytokinin (CK) and jasmonic acid (JA) implied their involvement in freezing stress responses. Collectively, these results suggested a critical role of DNA methylation in their transcriptional regulation in winter rapeseed under freezing stress.
Winter rapeseed is the largest source of edible oil in China and is especially sensitive to low temperature, which causes tremendous agricultural yield reduction and economic losses. It is still unclear how DNA methylation regulates the formation of freezing tolerance in winter rapeseed under freezing stress. Therefore, in this study, the whole-genome DNA methylation map and transcriptome expression profiles of freezing-resistant cultivar NTS57 (NS) under freezing stress were obtained. The genome-wide methylation assay exhibited lower levels of methylation in gene-rich regions. DNA methylation was identified in three genomic sequence contexts including CG, CHG and CHH, of which CG contexts exhibited the highest methylation levels (66.8%), followed by CHG (28.6%) and CHH (9.5%). Higher levels of the methylation were found in upstream 2 k and downstream 2 k of gene regions, whereas lowest levels were in the gene body regions. In addition, 331, 437, and 1720 unique differentially methylated genes (DMGs) were identified in three genomic sequence contexts in 17NS under freezing stress compared to the control. Function enrichment analysis suggested that most of enriched DMGs were involved in plant hormones signal transduction, phenylpropanoid biosynthesis and protein processing pathways. Changes of genes expression in signal transduction pathways for cytokinin (CK) and jasmonic acid (JA) implied their involvement in freezing stress responses. Collectively, these results suggested a critical role of DNA methylation in their transcriptional regulation in winter rapeseed under freezing stress.Winter rapeseed is the largest source of edible oil in China and is especially sensitive to low temperature, which causes tremendous agricultural yield reduction and economic losses. It is still unclear how DNA methylation regulates the formation of freezing tolerance in winter rapeseed under freezing stress. Therefore, in this study, the whole-genome DNA methylation map and transcriptome expression profiles of freezing-resistant cultivar NTS57 (NS) under freezing stress were obtained. The genome-wide methylation assay exhibited lower levels of methylation in gene-rich regions. DNA methylation was identified in three genomic sequence contexts including CG, CHG and CHH, of which CG contexts exhibited the highest methylation levels (66.8%), followed by CHG (28.6%) and CHH (9.5%). Higher levels of the methylation were found in upstream 2 k and downstream 2 k of gene regions, whereas lowest levels were in the gene body regions. In addition, 331, 437, and 1720 unique differentially methylated genes (DMGs) were identified in three genomic sequence contexts in 17NS under freezing stress compared to the control. Function enrichment analysis suggested that most of enriched DMGs were involved in plant hormones signal transduction, phenylpropanoid biosynthesis and protein processing pathways. Changes of genes expression in signal transduction pathways for cytokinin (CK) and jasmonic acid (JA) implied their involvement in freezing stress responses. Collectively, these results suggested a critical role of DNA methylation in their transcriptional regulation in winter rapeseed under freezing stress.
Author Zheng, Guoqiang
Dong, Xiaoyun
Wei, Jiaping
Shen, Yingzi
Wang, Ying
Li, Hui
Cui, Junmei
Liu, Zigang
Zhu, Yajing
Tian, Haiyan
AuthorAffiliation 1 State Key Laboratory of Aridland Crop Science , Lanzhou , China
4 Economic Crop Research Institute , Henan Academy of Agricultural Sciences , Zhengzhou , China
3 College of Agronomy , Gansu Agricultural University , Lanzhou , China
2 State Key Laboratory of Crop Genetics and Germplasm Enhancement , Nanjing Agricultural University , Nanjing , China
AuthorAffiliation_xml – name: 2 State Key Laboratory of Crop Genetics and Germplasm Enhancement , Nanjing Agricultural University , Nanjing , China
– name: 4 Economic Crop Research Institute , Henan Academy of Agricultural Sciences , Zhengzhou , China
– name: 1 State Key Laboratory of Aridland Crop Science , Lanzhou , China
– name: 3 College of Agronomy , Gansu Agricultural University , Lanzhou , China
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Cites_doi 10.1105/tpc.113.117796
10.1104/pp.16.00860
10.1093/bioinformatics/btp536
10.1073/pnas.1815441116
10.1038/s41467-020-19333-4
10.3390/ijms19124077
10.3389/fpls.2016.00936
10.3389/fpls.2020.00142
10.1186/s13059-016-1059-0
10.3389/fgene.2019.01222
10.1073/pnas.1107161108
10.1111/tpj.13790
10.1111/tpj.14512
10.1016/j.pbi.2017.01.005
10.1111/nph.14952
10.1016/j.cellsig.2012.01.008
10.4161/psb.6.11.17613
10.3390/ijms20205089
10.3390/ijms19113346
10.1093/jxb/erx004
10.1146/annurev-arplant-080720-093057
10.1111/pbi.13201
10.1073/pnas.1604666113
10.1016/j.tplants.2018.10.003
10.1093/nar/gkx417
10.1105/tpc.16.00669
10.1073/pnas.1515170112
10.1104/pp.15.00581
10.1111/tpj.15237
10.1104/pp.16.00533
10.3390/ijms20020243
10.1186/gb-2013-14-4-r36
10.1111/nph.17018
10.1111/ppl.12491
10.1038/s41580-018-0016-z
10.3389/fpls.2021.664311
10.1111/jipb.12706
10.1105/tpc.109.069906
10.1111/jipb.12614
10.1111/nph.15696
10.1093/nar/gkv1070
10.1093/jxb/erw496
10.1104/pp.113.232413
10.1038/nbt.1621
10.7554/eLife.37434
10.1007/s10725-021-00763-z
10.1111/tpj.12796
10.3390/ijms20112771
10.1016/j.molp.2020.02.004
10.1073/pnas.1705233114
10.1016/j.tplants.2018.04.002
10.1016/j.molp.2015.03.012
10.1111/pce.13953
10.1093/jxb/eraa576
10.1093/jxb/erv433
10.1093/jxb/erz470
10.4161/psb.21516
10.1111/pce.13579
10.1111/j.1365-313x.2010.04477.x
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content type line 23
Yang Yuting, Ninxia Unversity, China
Reviewed by: Jianfang Li, Guangzhou Laboratory, China
Edited by: Yuchen Yang, School of Ecology, Sun Yat-sen University, China
This article was submitted to Plant Genomics, a section of the journal Frontiers in Genetics
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References Ding (B9) 2020; 13
Liu (B28) 2021; 229
Wang (B46) 2018; 93
Deng (B7) 2015; 169
Zhang (B58) 2020; 71
Zhang (B57) 2015; 112
Pu (B34) 2019; 20
Liu (B27) 2015; 8
El-Sharkawy (B10) 2015; 66
Liu (B30) 2018; 60
Kanehisa (B21) 2016; 44
Xu (B53) 2020; 11
Nongpiur (B32) 2012; 7
Kollist (B25) 2019; 24
Ray (B36) 2012; 24
Chen (B6) 2020; 11
Tong (B44) 2021; 106
Saha (B38) 2016; 7
Wu (B51) 2019; 42
Shi (B41) 2018; 23
Shibasaki (B42) 2009; 21
Catalá (B5) 2011; 108
Wei (B48); 96
Binns (B4) 2009; 25
Park (B33) 2015; 82
Iwasaki (B20) 2019; 8
Huang (B19) 2016; 172
Guo (B13) 2019; 20
Kidokoro (B22) 2017; 29
Zhang (B56) 2018; 19
Kim (B24) 2017; 45
Ding (B8) 2019; 222
Wei (B49); 12
Folsom (B11) 2014; 165
Takahashi (B43) 2021; 44
Ramakrishna (B35) 2011; 6
Wang (B47) 2019; 10
Trapnell (B45) 2010; 28
Zeng (B55) 2018; 19
Zhao (B59) 2016; 171
An (B1) 2020; 18
Liu (B29) 2017; 68
Huang (B18) 2019; 116
Andrási (B2) 2021; 72
Lang (B26) 2017; 114
Ré (B37) 2017; 159
Seo (B39) 2011; 65
Witasari (B50) 2019; 100
Hemsley (B15) 2014; 26
Gao (B12) 2019; 20
Hoang (B16) 2021; 72
Kim (B23) 2013; 14
Xu (B54) 2018; 19
Xie (B52) 2018; 218
Hu (B17) 2017; 68
Seymour (B40) 2017; 36
Niederhuth (B31) 2016; 17
Guo (B14) 2018; 60
Bewick (B3) 2016; 113
References_xml – volume: 26
  start-page: 465
  year: 2014
  ident: B15
  article-title: The arabidopsis mediator complex subunits MED16, MED14, and MED2 regulate mediator and RNA polymerase II recruitment to CBF-responsive cold-regulated genes
  publication-title: Plant Cell
  doi: 10.1105/tpc.113.117796
– volume: 172
  start-page: 1182
  year: 2016
  ident: B19
  article-title: The heat stress factor HSFA6b connects ABA signaling and ABA-mediated heat responses
  publication-title: Plant Physiol.
  doi: 10.1104/pp.16.00860
– volume: 25
  start-page: 3045
  year: 2009
  ident: B4
  article-title: QuickGO: A web-based tool for gene Ontology searching
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btp536
– volume: 116
  start-page: 1430
  year: 2019
  ident: B18
  article-title: Global increase in DNA methylation during orange fruit development and ripening
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.1815441116
– volume: 11
  start-page: 5539
  year: 2020
  ident: B53
  article-title: Evolutionary and functional genomics of DNA methylation in maize domestication and improvement
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-020-19333-4
– volume: 19
  start-page: 4077
  year: 2018
  ident: B55
  article-title: iTRAQ-based comparative proteomic analysis of the roots of two winter turnip rapes (Brassica rapa L.) with different freezing-tolerance
  publication-title: Ijms
  doi: 10.3390/ijms19124077
– volume: 7
  start-page: 936
  year: 2016
  ident: B38
  article-title: A genome-wide analysis reveals stress and hormone responsive patterns of TIFY family genes in Brassica rapa
  publication-title: Front. Plant Sci.
  doi: 10.3389/fpls.2016.00936
– volume: 11
  start-page: 142
  year: 2020
  ident: B6
  article-title: SaHsfA4c from Sedum alfredii Hance enhances cadmium tolerance by regulating ROS-scavenger activities and heat shock proteins expression
  publication-title: Front. Plant Sci.
  doi: 10.3389/fpls.2020.00142
– volume: 17
  start-page: 194
  year: 2016
  ident: B31
  article-title: Widespread natural variation of DNA methylation within angiosperms
  publication-title: Genome Biol.
  doi: 10.1186/s13059-016-1059-0
– volume: 10
  start-page: 1222
  year: 2019
  ident: B47
  article-title: Molecular and phylogenetic analyses of the mediator subunit genes in Solanum lycopersicum
  publication-title: Front. Genet.
  doi: 10.3389/fgene.2019.01222
– volume: 108
  start-page: 16475
  year: 2011
  ident: B5
  article-title: Integration of low temperature and light signaling during cold acclimation response in Arabidopsis
  publication-title: Proc. Natl. Acad. Sci.
  doi: 10.1073/pnas.1107161108
– volume: 93
  start-page: 460
  year: 2018
  ident: B46
  article-title: Comparative epigenomics reveals evolution of duplicated genes in potato and tomato
  publication-title: Plant J.
  doi: 10.1111/tpj.13790
– volume: 100
  start-page: 1237
  year: 2019
  ident: B50
  article-title: Higher expression of the strawberry xyloglucan endotransglucosylase/hydrolase genesFvXTH9andFvXTH6accelerates fruit ripening
  publication-title: Plant J.
  doi: 10.1111/tpj.14512
– volume: 36
  start-page: 56
  year: 2017
  ident: B40
  article-title: The causes and consequences of DNA methylome variation in plants
  publication-title: Curr. Opin. Plant Biol.
  doi: 10.1016/j.pbi.2017.01.005
– volume: 218
  start-page: 201
  year: 2018
  ident: B52
  article-title: An atypical R2R3 MYB transcription factor increases cold hardiness by CBF-dependent and CBF-independent pathways in apple
  publication-title: New Phytol.
  doi: 10.1111/nph.14952
– volume: 24
  start-page: 981
  year: 2012
  ident: B36
  article-title: Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling
  publication-title: Cell. Signal.
  doi: 10.1016/j.cellsig.2012.01.008
– volume: 6
  start-page: 1720
  year: 2011
  ident: B35
  article-title: Influence of abiotic stress signals on secondary metabolites in plants
  publication-title: Plant Signal Behav.
  doi: 10.4161/psb.6.11.17613
– volume: 20
  start-page: 5089
  year: 2019
  ident: B13
  article-title: The methylation patterns and transcriptional responses to chilling stress at the seedling stage in rice
  publication-title: Ijms
  doi: 10.3390/ijms20205089
– volume: 19
  start-page: 3346
  year: 2018
  ident: B54
  article-title: iTRAQ-based quantitative proteome revealed metabolic changes in winter turnip rape (Brassica rapa L.) under cold stress
  publication-title: Ijms
  doi: 10.3390/ijms19113346
– volume: 68
  start-page: 1361
  year: 2017
  ident: B17
  article-title: Jasmonate regulates leaf senescence and tolerance to cold stress: Crosstalk with other phytohormones
  publication-title: J. Exp. Bot.
  doi: 10.1093/jxb/erx004
– volume: 72
  start-page: 297
  year: 2021
  ident: B16
  article-title: Histidine kinases: Diverse functions in plant development and responses to environmental conditions
  publication-title: Annu. Rev. Plant Biol.
  doi: 10.1146/annurev-arplant-080720-093057
– volume: 18
  start-page: 337
  year: 2020
  ident: B1
  article-title: An apple MYB transcription factor regulates cold tolerance and anthocyanin accumulation and undergoes MIEL1-mediated degradation
  publication-title: Plant Biotechnol. J.
  doi: 10.1111/pbi.13201
– volume: 113
  start-page: 9111
  year: 2016
  ident: B3
  article-title: On the origin and evolutionary consequences of gene body DNA methylation
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.1604666113
– volume: 24
  start-page: 25
  year: 2019
  ident: B25
  article-title: Rapid responses to abiotic stress: Priming the landscape for the signal transduction network
  publication-title: Trends Plant Sci.
  doi: 10.1016/j.tplants.2018.10.003
– volume: 45
  start-page: 6613
  year: 2017
  ident: B24
  article-title: Phosphorylation of the transcriptional repressor MYB15 by mitogen-activated protein kinase 6 is required for freezing tolerance in Arabidopsis
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkx417
– volume: 29
  start-page: 760
  year: 2017
  ident: B22
  article-title: Different cold-signaling pathways function in the responses to rapid and gradual decreases in temperature
  publication-title: Plant Cell
  doi: 10.1105/tpc.16.00669
– volume: 112
  start-page: 7022
  year: 2015
  ident: B57
  article-title: Autotetraploid rice methylome analysis reveals methylation variation of transposable elements and their effects on gene expression
  publication-title: Proc. Natl. Acad. Sci.
  doi: 10.1073/pnas.1515170112
– volume: 169
  start-page: 530
  year: 2015
  ident: B7
  article-title: Populus euphratica APYRASE2 enhances cold tolerance by modulating vesicular trafficking and extracellular ATP in Arabidopsis plants
  publication-title: Plant Physiol.
  doi: 10.1104/pp.15.00581
– volume: 106
  start-page: 1312
  year: 2021
  ident: B44
  article-title: Divergent DNA methylation contributes to duplicated gene evolution and chilling response in tea plants
  publication-title: Plant J.
  doi: 10.1111/tpj.15237
– volume: 171
  start-page: 2744
  year: 2016
  ident: B59
  article-title: Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis
  publication-title: Plant Physiol.
  doi: 10.1104/pp.16.00533
– volume: 20
  start-page: 243
  year: 2019
  ident: B12
  article-title: Quantitative proteomic analysis of the response to cold stress in Jojoba, a tropical woody crop
  publication-title: Ijms
  doi: 10.3390/ijms20020243
– volume: 14
  start-page: 36
  year: 2013
  ident: B23
  article-title: TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
  publication-title: Genome Biol.
  doi: 10.1186/gb-2013-14-4-r36
– volume: 229
  start-page: 2238
  year: 2021
  ident: B28
  article-title: Role of H1 and DNA methylation in selective regulation of transposable elements during heat stress
  publication-title: New Phytol.
  doi: 10.1111/nph.17018
– volume: 159
  start-page: 148
  year: 2017
  ident: B37
  article-title: Small heat shock proteins and the postharvest chilling tolerance of tomato fruit
  publication-title: Physiol. Plant
  doi: 10.1111/ppl.12491
– volume: 19
  start-page: 489
  year: 2018
  ident: B56
  article-title: Dynamics and function of DNA methylation in plants
  publication-title: Nat. Rev. Mol. Cell Biol.
  doi: 10.1038/s41580-018-0016-z
– volume: 12
  start-page: 664311
  ident: B49
  article-title: Comparative transcriptomics and proteomics analyses of leaves reveals a freezing stress-responsive molecular network in winter rapeseed (Brassica rapa L.)
  publication-title: Front. Plant Sci.
  doi: 10.3389/fpls.2021.664311
– volume: 60
  start-page: 745
  year: 2018
  ident: B14
  article-title: Cold signaling in plants: Insights into mechanisms and regulation
  publication-title: J. Integr. Plant Biol.
  doi: 10.1111/jipb.12706
– volume: 21
  start-page: 3823
  year: 2009
  ident: B42
  article-title: Auxin response inArabidopsisunder cold stress: Underlying molecular mechanisms
  publication-title: Plant Cell
  doi: 10.1105/tpc.109.069906
– volume: 60
  start-page: 173
  year: 2018
  ident: B30
  article-title: The calcium-dependent kinase OsCPK24 functions in cold stress responses in rice
  publication-title: J. Integr. Plant Biol.
  doi: 10.1111/jipb.12614
– volume: 222
  start-page: 1690
  year: 2019
  ident: B8
  article-title: Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants
  publication-title: New Phytol.
  doi: 10.1111/nph.15696
– volume: 44
  start-page: 457
  year: 2016
  ident: B21
  article-title: KEGG as a reference resource for gene and protein annotation
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkv1070
– volume: 68
  start-page: 1213
  year: 2017
  ident: B29
  article-title: Cold acclimation alters DNA methylation patterns and confers tolerance to heat and increases growth rate in Brassica rapa
  publication-title: J. Exp. Bot.
  doi: 10.1093/jxb/erw496
– volume: 165
  start-page: 238
  year: 2014
  ident: B11
  article-title: Rice fertilization-independent Endosperm1 regulates seed size under heat stress by controlling early endosperm development
  publication-title: Plant Physiol.
  doi: 10.1104/pp.113.232413
– volume: 28
  start-page: 511
  year: 2010
  ident: B45
  article-title: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation
  publication-title: Nat. Biotechnol.
  doi: 10.1038/nbt.1621
– volume: 8
  start-page: e37434
  year: 2019
  ident: B20
  article-title: Non-canonical RNA-directed DNA methylation participates in maternal and environmental control of seed dormancy
  publication-title: eLife
  doi: 10.7554/eLife.37434
– volume: 96
  start-page: 103
  ident: B48
  article-title: Integration of transcriptome and proteome analysis reveals the mechanism of freezing tolerance in winter rapeseed
  publication-title: Plant Growth Regul.
  doi: 10.1007/s10725-021-00763-z
– volume: 82
  start-page: 193
  year: 2015
  ident: B33
  article-title: Regulation of the Arabidopsis CBF regulon by a complex low‐temperature regulatory network
  publication-title: Plant J.
  doi: 10.1111/tpj.12796
– volume: 20
  start-page: 2771
  year: 2019
  ident: B34
  article-title: Transcriptome profile analysis of winter rapeseed (Brassica napus L.) in response to freezing stress, reveal potentially connected events to freezing stress
  publication-title: Ijms
  doi: 10.3390/ijms20112771
– volume: 13
  start-page: 544
  year: 2020
  ident: B9
  article-title: Molecular regulation of plant responses to environmental temperatures
  publication-title: Mol. Plant
  doi: 10.1016/j.molp.2020.02.004
– volume: 114
  start-page: 4511
  year: 2017
  ident: B26
  article-title: Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit
  publication-title: Proc. Natl. Acad. Sci.
  doi: 10.1073/pnas.1705233114
– volume: 23
  start-page: 623
  year: 2018
  ident: B41
  article-title: Molecular regulation of CBF signaling in cold acclimation
  publication-title: Trends Plant Sci.
  doi: 10.1016/j.tplants.2018.04.002
– volume: 8
  start-page: 689
  year: 2015
  ident: B27
  article-title: MYB transcription factors as regulators of phenylpropanoid metabolism in plants
  publication-title: Mol. Plant
  doi: 10.1016/j.molp.2015.03.012
– volume: 44
  start-page: 915
  year: 2021
  ident: B43
  article-title: Cell wall modification by the xyloglucan endotransglucosylase/hydrolase XTH19 influences freezing tolerance after cold and sub‐zero acclimation
  publication-title: Plant Cell Environ.
  doi: 10.1111/pce.13953
– volume: 72
  start-page: 1558
  year: 2021
  ident: B2
  article-title: Diversity of plant heat shock factors: Regulation, interactions, and functions
  publication-title: J. Exp. Bot.
  doi: 10.1093/jxb/eraa576
– volume: 66
  start-page: 7359
  year: 2015
  ident: B10
  article-title: Transcriptome analysis of an apple (Malus×domestica) yellow fruit somatic mutation identifies a gene network module highly associated with anthocyanin and epigenetic regulation
  publication-title: Exbotj
  doi: 10.1093/jxb/erv433
– volume: 71
  start-page: 951
  year: 2020
  ident: B58
  article-title: Single-base resolution methylome of cotton cytoplasmic male sterility system reveals epigenomic changes in response to high-temperature stress during anther development
  publication-title: J. Exp. Bot.
  doi: 10.1093/jxb/erz470
– volume: 7
  start-page: 1230
  year: 2012
  ident: B32
  article-title: Histidine kinases in plants
  publication-title: Plant Signal. Behav.
  doi: 10.4161/psb.21516
– volume: 42
  start-page: 2645
  year: 2019
  ident: B51
  article-title: Cold stress activates disease resistance inArabidopsis thalianathrough a salicylic acid dependent pathway
  publication-title: Plant Cell Environ.
  doi: 10.1111/pce.13579
– volume: 65
  start-page: 907
  year: 2011
  ident: B39
  article-title: OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice
  publication-title: Plant J.
  doi: 10.1111/j.1365-313x.2010.04477.x
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Snippet Winter rapeseed is the largest source of edible oil in China and is especially sensitive to low temperature, which causes tremendous agricultural yield...
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SubjectTerms differentially methylated genes
DNA methylation
freezing stress
Genetics
transcriptome
winter rapeseed
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Title DNA methylation affects freezing tolerance in winter rapeseed by mediating the expression of genes related to JA and CK pathways
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https://pubmed.ncbi.nlm.nih.gov/PMC9432081
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