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Single-base resolution methylome of different ecotype from Pyrus betulaefolia reveals epigenomic changes in response to salt stress

•Drawing the cytosine methylation map across the whole genome of Pyrus betulaefolia roots.•The changes of methylomes in two ecotypes after salt exposed dependent on their salt tolerance abilities.•DNA demethylation induced higher expression levels of some Ca2+ sensor genes in P. betulaefolia roots.•...

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Published in:Scientia horticulturae 2022-12, Vol.306, p.111437, Article 111437
Main Authors: Li, Hui, Zhang, Yu-feng, Zhou, Xiang-yang, Lin, Jin, Liu, Chun-xiao, Li, Xiao-gang, Chang, You-hong
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Zhou, Xiang-yang
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Li, Xiao-gang
Chang, You-hong
description •Drawing the cytosine methylation map across the whole genome of Pyrus betulaefolia roots.•The changes of methylomes in two ecotypes after salt exposed dependent on their salt tolerance abilities.•DNA demethylation induced higher expression levels of some Ca2+ sensor genes in P. betulaefolia roots.•The higher K+/Na+ ratio in the roots of salt-tolerance ecotype is relationship with Ca2+ sensor genes transcription causing by hypomethylation. The root is the first organ to feel salt stress in woody fruit trees. Understanding the potential epigenetic mechanism induced by salt stress in roots of Pyrus betulaefolia is important for pear breeding using diverse genetic resources. With the help of whole-genome bisulfite sequencing, cytosine methylation was mapped at single-base resolution across the whole genome of P. betulaefolia roots. The P. betulaefolia root genome revealed nearly 11.40%, 39.93%, 22.73%, and 4.17% methylation across all sequenced C sites and in the CG, CHG, and CHH sequence contexts, respectively. Then, the changes in the methylome of the roots relating to salt stress were comparatively analysed in two ecotypes with different salt-stress tolerances. After a global methylome and transcriptome combined analysis, gene body methylation demonstrated an obvious negative correlation with transcription levels, whereas promoter-methylated genes presented lower expression levels than promoter-unmethylated genes. Furthermore, the methylation profiles of Ca2+ sensor genes in roots of P. betulaefolia. were described, and some were demethylated under salt-stress conditions. In detail, the up-regulation of Ca2+ sensors and their downstream genes, PbCDPK20.1, PbCDPK20.2, PbAKT1, and PbHAK25, resulted from salt-induced promoter methylation changes. Finally, K+ accumulation was promoted, and a higher K+/Na+ratio was maintained in roots under salt-stress compared with normal conditions. Additionally, the application of the DNA methylation inhibitor 5-azacytidine in vitro induced DNA demethylation and promoted K+ enrichment, whereas the accelerator methyl trifluoromethanesulfonate produced the opposite effects. In conclusion, our result revealed the relationship of DNA methylation and gene expression in P. betulaefolia during salt stress, which will increase our understanding of the epigenetic mechanisms of woody trees.
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The root is the first organ to feel salt stress in woody fruit trees. Understanding the potential epigenetic mechanism induced by salt stress in roots of Pyrus betulaefolia is important for pear breeding using diverse genetic resources. With the help of whole-genome bisulfite sequencing, cytosine methylation was mapped at single-base resolution across the whole genome of P. betulaefolia roots. The P. betulaefolia root genome revealed nearly 11.40%, 39.93%, 22.73%, and 4.17% methylation across all sequenced C sites and in the CG, CHG, and CHH sequence contexts, respectively. Then, the changes in the methylome of the roots relating to salt stress were comparatively analysed in two ecotypes with different salt-stress tolerances. After a global methylome and transcriptome combined analysis, gene body methylation demonstrated an obvious negative correlation with transcription levels, whereas promoter-methylated genes presented lower expression levels than promoter-unmethylated genes. Furthermore, the methylation profiles of Ca2+ sensor genes in roots of P. betulaefolia. were described, and some were demethylated under salt-stress conditions. In detail, the up-regulation of Ca2+ sensors and their downstream genes, PbCDPK20.1, PbCDPK20.2, PbAKT1, and PbHAK25, resulted from salt-induced promoter methylation changes. Finally, K+ accumulation was promoted, and a higher K+/Na+ratio was maintained in roots under salt-stress compared with normal conditions. Additionally, the application of the DNA methylation inhibitor 5-azacytidine in vitro induced DNA demethylation and promoted K+ enrichment, whereas the accelerator methyl trifluoromethanesulfonate produced the opposite effects. In conclusion, our result revealed the relationship of DNA methylation and gene expression in P. betulaefolia during salt stress, which will increase our understanding of the epigenetic mechanisms of woody trees.</description><identifier>ISSN: 0304-4238</identifier><identifier>EISSN: 1879-1018</identifier><identifier>DOI: 10.1016/j.scienta.2022.111437</identifier><language>eng</language><publisher>Elsevier B.V</publisher><subject>bisulfites ; Ca2+ sensor gene ; calcium ; DNA demethylation ; DNA methylation ; ecotypes ; epigenetics ; epigenome ; fruits ; gene expression ; genes ; Methylome ; pears ; Pyrus betulaefolia ; Pyrus betulifolia ; Salt stress ; Sodium-potassium balance ; Transcriptome</subject><ispartof>Scientia horticulturae, 2022-12, Vol.306, p.111437, Article 111437</ispartof><rights>2022 Elsevier B.V.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c290t-2d2d2bc6fa10203ea5cd78634f8a445a4695f63a294188ca2c174c0d594344943</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,777,781,27905,27906</link.rule.ids></links><search><creatorcontrib>Li, Hui</creatorcontrib><creatorcontrib>Zhang, Yu-feng</creatorcontrib><creatorcontrib>Zhou, Xiang-yang</creatorcontrib><creatorcontrib>Lin, Jin</creatorcontrib><creatorcontrib>Liu, Chun-xiao</creatorcontrib><creatorcontrib>Li, Xiao-gang</creatorcontrib><creatorcontrib>Chang, You-hong</creatorcontrib><title>Single-base resolution methylome of different ecotype from Pyrus betulaefolia reveals epigenomic changes in response to salt stress</title><title>Scientia horticulturae</title><description>•Drawing the cytosine methylation map across the whole genome of Pyrus betulaefolia roots.•The changes of methylomes in two ecotypes after salt exposed dependent on their salt tolerance abilities.•DNA demethylation induced higher expression levels of some Ca2+ sensor genes in P. betulaefolia roots.•The higher K+/Na+ ratio in the roots of salt-tolerance ecotype is relationship with Ca2+ sensor genes transcription causing by hypomethylation. The root is the first organ to feel salt stress in woody fruit trees. Understanding the potential epigenetic mechanism induced by salt stress in roots of Pyrus betulaefolia is important for pear breeding using diverse genetic resources. With the help of whole-genome bisulfite sequencing, cytosine methylation was mapped at single-base resolution across the whole genome of P. betulaefolia roots. The P. betulaefolia root genome revealed nearly 11.40%, 39.93%, 22.73%, and 4.17% methylation across all sequenced C sites and in the CG, CHG, and CHH sequence contexts, respectively. Then, the changes in the methylome of the roots relating to salt stress were comparatively analysed in two ecotypes with different salt-stress tolerances. After a global methylome and transcriptome combined analysis, gene body methylation demonstrated an obvious negative correlation with transcription levels, whereas promoter-methylated genes presented lower expression levels than promoter-unmethylated genes. Furthermore, the methylation profiles of Ca2+ sensor genes in roots of P. betulaefolia. were described, and some were demethylated under salt-stress conditions. In detail, the up-regulation of Ca2+ sensors and their downstream genes, PbCDPK20.1, PbCDPK20.2, PbAKT1, and PbHAK25, resulted from salt-induced promoter methylation changes. Finally, K+ accumulation was promoted, and a higher K+/Na+ratio was maintained in roots under salt-stress compared with normal conditions. Additionally, the application of the DNA methylation inhibitor 5-azacytidine in vitro induced DNA demethylation and promoted K+ enrichment, whereas the accelerator methyl trifluoromethanesulfonate produced the opposite effects. In conclusion, our result revealed the relationship of DNA methylation and gene expression in P. betulaefolia during salt stress, which will increase our understanding of the epigenetic mechanisms of woody trees.</description><subject>bisulfites</subject><subject>Ca2+ sensor gene</subject><subject>calcium</subject><subject>DNA demethylation</subject><subject>DNA methylation</subject><subject>ecotypes</subject><subject>epigenetics</subject><subject>epigenome</subject><subject>fruits</subject><subject>gene expression</subject><subject>genes</subject><subject>Methylome</subject><subject>pears</subject><subject>Pyrus betulaefolia</subject><subject>Pyrus betulifolia</subject><subject>Salt stress</subject><subject>Sodium-potassium balance</subject><subject>Transcriptome</subject><issn>0304-4238</issn><issn>1879-1018</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNqFkE1LAzEQhoMoWKs_QcjRy9Ykm_06iRS_oKCgnkOanbQp2c2aZAs9-8dN2d5lYAaG532HeRG6pWRBCS3vd4ugDPRRLhhhbEEp5Xl1hma0rposEfU5mpGc8IyzvL5EVyHsCCGJambo99P0GwvZWgbAHoKzYzSuxx3E7cG6DrDTuDVag08XMCgXDwNg7V2HPw5-DHgNcbQStLNGJoc9SBswDGYDveuMwmor-w0EbPqj_-D6dCg6HKSNOMS0CtfoQicR3JzmHH0_P30tX7PV-8vb8nGVKdaQmLE21VqVWlLCSA6yUG1VlznXteS8kLxsCl3mkjWc1rWSTNGKK9IWDc85T22O7ibfwbufEUIUnQkKrJU9uDEIVtE6LxlpmoQWE6q8C8GDFoM3nfQHQYk4hi524hS6OIYuptCT7mHSQfpjb8BPlILWeFBRtM784_AHOPOQDQ</recordid><startdate>20221215</startdate><enddate>20221215</enddate><creator>Li, Hui</creator><creator>Zhang, Yu-feng</creator><creator>Zhou, Xiang-yang</creator><creator>Lin, Jin</creator><creator>Liu, Chun-xiao</creator><creator>Li, Xiao-gang</creator><creator>Chang, You-hong</creator><general>Elsevier B.V</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>20221215</creationdate><title>Single-base resolution methylome of different ecotype from Pyrus betulaefolia reveals epigenomic changes in response to salt stress</title><author>Li, Hui ; Zhang, Yu-feng ; Zhou, Xiang-yang ; Lin, Jin ; Liu, Chun-xiao ; Li, Xiao-gang ; Chang, You-hong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c290t-2d2d2bc6fa10203ea5cd78634f8a445a4695f63a294188ca2c174c0d594344943</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>bisulfites</topic><topic>Ca2+ sensor gene</topic><topic>calcium</topic><topic>DNA demethylation</topic><topic>DNA methylation</topic><topic>ecotypes</topic><topic>epigenetics</topic><topic>epigenome</topic><topic>fruits</topic><topic>gene expression</topic><topic>genes</topic><topic>Methylome</topic><topic>pears</topic><topic>Pyrus betulaefolia</topic><topic>Pyrus betulifolia</topic><topic>Salt stress</topic><topic>Sodium-potassium balance</topic><topic>Transcriptome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Hui</creatorcontrib><creatorcontrib>Zhang, Yu-feng</creatorcontrib><creatorcontrib>Zhou, Xiang-yang</creatorcontrib><creatorcontrib>Lin, Jin</creatorcontrib><creatorcontrib>Liu, Chun-xiao</creatorcontrib><creatorcontrib>Li, Xiao-gang</creatorcontrib><creatorcontrib>Chang, You-hong</creatorcontrib><collection>CrossRef</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Scientia horticulturae</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Hui</au><au>Zhang, Yu-feng</au><au>Zhou, Xiang-yang</au><au>Lin, Jin</au><au>Liu, Chun-xiao</au><au>Li, Xiao-gang</au><au>Chang, You-hong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Single-base resolution methylome of different ecotype from Pyrus betulaefolia reveals epigenomic changes in response to salt stress</atitle><jtitle>Scientia horticulturae</jtitle><date>2022-12-15</date><risdate>2022</risdate><volume>306</volume><spage>111437</spage><pages>111437-</pages><artnum>111437</artnum><issn>0304-4238</issn><eissn>1879-1018</eissn><abstract>•Drawing the cytosine methylation map across the whole genome of Pyrus betulaefolia roots.•The changes of methylomes in two ecotypes after salt exposed dependent on their salt tolerance abilities.•DNA demethylation induced higher expression levels of some Ca2+ sensor genes in P. betulaefolia roots.•The higher K+/Na+ ratio in the roots of salt-tolerance ecotype is relationship with Ca2+ sensor genes transcription causing by hypomethylation. The root is the first organ to feel salt stress in woody fruit trees. Understanding the potential epigenetic mechanism induced by salt stress in roots of Pyrus betulaefolia is important for pear breeding using diverse genetic resources. With the help of whole-genome bisulfite sequencing, cytosine methylation was mapped at single-base resolution across the whole genome of P. betulaefolia roots. The P. betulaefolia root genome revealed nearly 11.40%, 39.93%, 22.73%, and 4.17% methylation across all sequenced C sites and in the CG, CHG, and CHH sequence contexts, respectively. Then, the changes in the methylome of the roots relating to salt stress were comparatively analysed in two ecotypes with different salt-stress tolerances. After a global methylome and transcriptome combined analysis, gene body methylation demonstrated an obvious negative correlation with transcription levels, whereas promoter-methylated genes presented lower expression levels than promoter-unmethylated genes. Furthermore, the methylation profiles of Ca2+ sensor genes in roots of P. betulaefolia. were described, and some were demethylated under salt-stress conditions. In detail, the up-regulation of Ca2+ sensors and their downstream genes, PbCDPK20.1, PbCDPK20.2, PbAKT1, and PbHAK25, resulted from salt-induced promoter methylation changes. Finally, K+ accumulation was promoted, and a higher K+/Na+ratio was maintained in roots under salt-stress compared with normal conditions. Additionally, the application of the DNA methylation inhibitor 5-azacytidine in vitro induced DNA demethylation and promoted K+ enrichment, whereas the accelerator methyl trifluoromethanesulfonate produced the opposite effects. In conclusion, our result revealed the relationship of DNA methylation and gene expression in P. betulaefolia during salt stress, which will increase our understanding of the epigenetic mechanisms of woody trees.</abstract><pub>Elsevier B.V</pub><doi>10.1016/j.scienta.2022.111437</doi></addata></record>
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subjects bisulfites
Ca2+ sensor gene
calcium
DNA demethylation
DNA methylation
ecotypes
epigenetics
epigenome
fruits
gene expression
genes
Methylome
pears
Pyrus betulaefolia
Pyrus betulifolia
Salt stress
Sodium-potassium balance
Transcriptome
title Single-base resolution methylome of different ecotype from Pyrus betulaefolia reveals epigenomic changes in response to salt stress
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