Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice ( Oryza sativa L.)
Cytosine methylation is responsive to various biotic- and abiotic-stresses, which may produce heritable epialleles. Nitrogen (N)-deficiency is an abiotic stress being repeatedly experienced by plants. To address possible epigenetic consequences of N-deficiency-stress, we investigated the stability o...
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| Veröffentlicht in: | Journal of plant physiology 2011-09, Vol.168 (14), p.1685-1693 |
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| creator | Kou, H.P. Li, Y. Song, X.X. Ou, X.F. Xing, S.C. Ma, J. Von Wettstein, D. Liu, B. |
| description | Cytosine methylation is responsive to various biotic- and abiotic-stresses, which may produce heritable epialleles. Nitrogen (N)-deficiency is an abiotic stress being repeatedly experienced by plants. To address possible epigenetic consequences of N-deficiency-stress, we investigated the stability of cytosine methylation in rice (
Oryza sativa L.) subsequent to a chronic (a whole-generation) N-deficiency at two levels, moderate (20
mg/L) and severe (10
mg/L), under hydroponic culture. MSAP analysis revealed that locus-specific methylation alteration occurred in leaf-tissue of the stressed plants (S
0) experiencing either level of N-deficiency, which was validated by gel-blotting. Analysis on three non-stressed self-fed progenies (S
1, S
2 and S
3) by gel-blotting indicated that
ca. 50% of the altered methylation patterns in somatic cells (leaf) of the stressed S
0 plants were recaptured in S
1, which were then stably inherited to S
2 and S
3. Bisulfite sequencing of two variant MSAP loci with homology to low-copy retrotransposons on one stressed plant (S
0) and its non-stressed progenies (S
1 and S
2) showed that whereas one locus exhibited limited and non-heritable CHH methylation alteration, the other locus manifested dramatic heritable hypermethylation at nearly all cytosine sites within the assayed region. Intriguingly, when two groups of S
2 plants descended from the same N-deficiency-stressed S
0 plant were re-subjected to the stress, the group inheriting the modified methylation patterns showed enhanced tolerance to the N-deficiency-stress compared with the group bearing the original patterns. Our results thus demonstrate heritability of an acquired adaptive trait in rice, which was accompanied by epigenetic inheritance of modified cytosine methylation patterns, implicating an epigenetic basis underlying the inheritance of an acquired trait in plants. |
| doi_str_mv | 10.1016/j.jplph.2011.03.017 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_907173828</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S017616171100229X</els_id><sourcerecordid>907173828</sourcerecordid><originalsourceid>FETCH-LOGICAL-c486t-1087bb96b0928a7c410e1c7ab9ac54e63577b55826de4fd05af634a7bd5d6b2c3</originalsourceid><addsrcrecordid>eNqFkcuOFCEUhonROO3oE5gYNkZdVAlFFdALF5NxxjHpOBtdEy6nbDp1E-hJysfxSaX6ojtdAYfv_8_J-RF6SUlJCeXvd-Vu6qZtWRFKS8JKQsUjtKKcyoKySj5Gq1zhRS6IC_Qsxh3J70ayp-iiopw3rGpW6NcdBJ-06QDrLkHQyY8D9gP--OUK95C2c3cuub0Fh82MB5_C-B2GwkHrrYfBzjimADFibe3YT3rwEDEMWz0skjR22ThfF_F0kC7_acRpC2dlbhl8Rt7i-zD_1Djmtg8ab8p3z9GTVncRXpzOS_Tt9ubr9V2xuf_0-fpqU9ha8lRQIoUxa27IupJa2JoSoFZos9a2qYGzRgjTNLLiDurWkUa3nNVaGNc4birLLtGbo28e8cceYlK9jxa6Tg8w7qNaE0EFk5X8LymFJJUUa5pJdiRtGGMM0Kop-F6HWVGilhTVTh1SVEuKijCVM8qqVyf_venB_dGcY8vA6xOgo9Vdu2zXx79czQRhzdL-w5GDvLcHD0HFQ17gfACblBv9Pwf5DXFSvjo</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>878028791</pqid></control><display><type>article</type><title>Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice ( Oryza sativa L.)</title><source>MEDLINE</source><source>Elsevier ScienceDirect Journals</source><creator>Kou, H.P. ; Li, Y. ; Song, X.X. ; Ou, X.F. ; Xing, S.C. ; Ma, J. ; Von Wettstein, D. ; Liu, B.</creator><creatorcontrib>Kou, H.P. ; Li, Y. ; Song, X.X. ; Ou, X.F. ; Xing, S.C. ; Ma, J. ; Von Wettstein, D. ; Liu, B.</creatorcontrib><description>Cytosine methylation is responsive to various biotic- and abiotic-stresses, which may produce heritable epialleles. Nitrogen (N)-deficiency is an abiotic stress being repeatedly experienced by plants. To address possible epigenetic consequences of N-deficiency-stress, we investigated the stability of cytosine methylation in rice (
Oryza sativa L.) subsequent to a chronic (a whole-generation) N-deficiency at two levels, moderate (20
mg/L) and severe (10
mg/L), under hydroponic culture. MSAP analysis revealed that locus-specific methylation alteration occurred in leaf-tissue of the stressed plants (S
0) experiencing either level of N-deficiency, which was validated by gel-blotting. Analysis on three non-stressed self-fed progenies (S
1, S
2 and S
3) by gel-blotting indicated that
ca. 50% of the altered methylation patterns in somatic cells (leaf) of the stressed S
0 plants were recaptured in S
1, which were then stably inherited to S
2 and S
3. Bisulfite sequencing of two variant MSAP loci with homology to low-copy retrotransposons on one stressed plant (S
0) and its non-stressed progenies (S
1 and S
2) showed that whereas one locus exhibited limited and non-heritable CHH methylation alteration, the other locus manifested dramatic heritable hypermethylation at nearly all cytosine sites within the assayed region. Intriguingly, when two groups of S
2 plants descended from the same N-deficiency-stressed S
0 plant were re-subjected to the stress, the group inheriting the modified methylation patterns showed enhanced tolerance to the N-deficiency-stress compared with the group bearing the original patterns. Our results thus demonstrate heritability of an acquired adaptive trait in rice, which was accompanied by epigenetic inheritance of modified cytosine methylation patterns, implicating an epigenetic basis underlying the inheritance of an acquired trait in plants.</description><identifier>ISSN: 0176-1617</identifier><identifier>EISSN: 1618-1328</identifier><identifier>DOI: 10.1016/j.jplph.2011.03.017</identifier><identifier>PMID: 21665325</identifier><identifier>CODEN: JPPHEY</identifier><language>eng</language><publisher>Munich: Elsevier GmbH</publisher><subject>Abiotic stress ; Adaptation ; Adaptation, Biological - genetics ; Biological and medical sciences ; Cytosine - metabolism ; Cytosine methylation alteration ; DNA Methylation - genetics ; DNA, Plant - genetics ; Epigenesis, Genetic - genetics ; Epigenetic inheritance ; Fundamental and applied biological sciences. Psychology ; Genetic Loci ; Hydroponics ; Inheritance Patterns ; Lamarckism ; Nitrogen (N)-deficiency ; Nitrogen - deficiency ; Nitrogen - metabolism ; Oryza - genetics ; Oryza - growth & development ; Oryza sativa ; Oryza sativa L ; Phenotype ; Plant physiology and development ; Stress, Physiological</subject><ispartof>Journal of plant physiology, 2011-09, Vol.168 (14), p.1685-1693</ispartof><rights>2011 Elsevier GmbH</rights><rights>2015 INIST-CNRS</rights><rights>Copyright © 2011 Elsevier GmbH. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c486t-1087bb96b0928a7c410e1c7ab9ac54e63577b55826de4fd05af634a7bd5d6b2c3</citedby><cites>FETCH-LOGICAL-c486t-1087bb96b0928a7c410e1c7ab9ac54e63577b55826de4fd05af634a7bd5d6b2c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S017616171100229X$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65534</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=24370351$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21665325$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kou, H.P.</creatorcontrib><creatorcontrib>Li, Y.</creatorcontrib><creatorcontrib>Song, X.X.</creatorcontrib><creatorcontrib>Ou, X.F.</creatorcontrib><creatorcontrib>Xing, S.C.</creatorcontrib><creatorcontrib>Ma, J.</creatorcontrib><creatorcontrib>Von Wettstein, D.</creatorcontrib><creatorcontrib>Liu, B.</creatorcontrib><title>Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice ( Oryza sativa L.)</title><title>Journal of plant physiology</title><addtitle>J Plant Physiol</addtitle><description>Cytosine methylation is responsive to various biotic- and abiotic-stresses, which may produce heritable epialleles. Nitrogen (N)-deficiency is an abiotic stress being repeatedly experienced by plants. To address possible epigenetic consequences of N-deficiency-stress, we investigated the stability of cytosine methylation in rice (
Oryza sativa L.) subsequent to a chronic (a whole-generation) N-deficiency at two levels, moderate (20
mg/L) and severe (10
mg/L), under hydroponic culture. MSAP analysis revealed that locus-specific methylation alteration occurred in leaf-tissue of the stressed plants (S
0) experiencing either level of N-deficiency, which was validated by gel-blotting. Analysis on three non-stressed self-fed progenies (S
1, S
2 and S
3) by gel-blotting indicated that
ca. 50% of the altered methylation patterns in somatic cells (leaf) of the stressed S
0 plants were recaptured in S
1, which were then stably inherited to S
2 and S
3. Bisulfite sequencing of two variant MSAP loci with homology to low-copy retrotransposons on one stressed plant (S
0) and its non-stressed progenies (S
1 and S
2) showed that whereas one locus exhibited limited and non-heritable CHH methylation alteration, the other locus manifested dramatic heritable hypermethylation at nearly all cytosine sites within the assayed region. Intriguingly, when two groups of S
2 plants descended from the same N-deficiency-stressed S
0 plant were re-subjected to the stress, the group inheriting the modified methylation patterns showed enhanced tolerance to the N-deficiency-stress compared with the group bearing the original patterns. Our results thus demonstrate heritability of an acquired adaptive trait in rice, which was accompanied by epigenetic inheritance of modified cytosine methylation patterns, implicating an epigenetic basis underlying the inheritance of an acquired trait in plants.</description><subject>Abiotic stress</subject><subject>Adaptation</subject><subject>Adaptation, Biological - genetics</subject><subject>Biological and medical sciences</subject><subject>Cytosine - metabolism</subject><subject>Cytosine methylation alteration</subject><subject>DNA Methylation - genetics</subject><subject>DNA, Plant - genetics</subject><subject>Epigenesis, Genetic - genetics</subject><subject>Epigenetic inheritance</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Genetic Loci</subject><subject>Hydroponics</subject><subject>Inheritance Patterns</subject><subject>Lamarckism</subject><subject>Nitrogen (N)-deficiency</subject><subject>Nitrogen - deficiency</subject><subject>Nitrogen - metabolism</subject><subject>Oryza - genetics</subject><subject>Oryza - growth & development</subject><subject>Oryza sativa</subject><subject>Oryza sativa L</subject><subject>Phenotype</subject><subject>Plant physiology and development</subject><subject>Stress, Physiological</subject><issn>0176-1617</issn><issn>1618-1328</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkcuOFCEUhonROO3oE5gYNkZdVAlFFdALF5NxxjHpOBtdEy6nbDp1E-hJysfxSaX6ojtdAYfv_8_J-RF6SUlJCeXvd-Vu6qZtWRFKS8JKQsUjtKKcyoKySj5Gq1zhRS6IC_Qsxh3J70ayp-iiopw3rGpW6NcdBJ-06QDrLkHQyY8D9gP--OUK95C2c3cuub0Fh82MB5_C-B2GwkHrrYfBzjimADFibe3YT3rwEDEMWz0skjR22ThfF_F0kC7_acRpC2dlbhl8Rt7i-zD_1Djmtg8ab8p3z9GTVncRXpzOS_Tt9ubr9V2xuf_0-fpqU9ha8lRQIoUxa27IupJa2JoSoFZos9a2qYGzRgjTNLLiDurWkUa3nNVaGNc4birLLtGbo28e8cceYlK9jxa6Tg8w7qNaE0EFk5X8LymFJJUUa5pJdiRtGGMM0Kop-F6HWVGilhTVTh1SVEuKijCVM8qqVyf_venB_dGcY8vA6xOgo9Vdu2zXx79czQRhzdL-w5GDvLcHD0HFQ17gfACblBv9Pwf5DXFSvjo</recordid><startdate>20110915</startdate><enddate>20110915</enddate><creator>Kou, H.P.</creator><creator>Li, Y.</creator><creator>Song, X.X.</creator><creator>Ou, X.F.</creator><creator>Xing, S.C.</creator><creator>Ma, J.</creator><creator>Von Wettstein, D.</creator><creator>Liu, B.</creator><general>Elsevier GmbH</general><general>Elsevier</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7TM</scope></search><sort><creationdate>20110915</creationdate><title>Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice ( Oryza sativa L.)</title><author>Kou, H.P. ; Li, Y. ; Song, X.X. ; Ou, X.F. ; Xing, S.C. ; Ma, J. ; Von Wettstein, D. ; Liu, B.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c486t-1087bb96b0928a7c410e1c7ab9ac54e63577b55826de4fd05af634a7bd5d6b2c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Abiotic stress</topic><topic>Adaptation</topic><topic>Adaptation, Biological - genetics</topic><topic>Biological and medical sciences</topic><topic>Cytosine - metabolism</topic><topic>Cytosine methylation alteration</topic><topic>DNA Methylation - genetics</topic><topic>DNA, Plant - genetics</topic><topic>Epigenesis, Genetic - genetics</topic><topic>Epigenetic inheritance</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Genetic Loci</topic><topic>Hydroponics</topic><topic>Inheritance Patterns</topic><topic>Lamarckism</topic><topic>Nitrogen (N)-deficiency</topic><topic>Nitrogen - deficiency</topic><topic>Nitrogen - metabolism</topic><topic>Oryza - genetics</topic><topic>Oryza - growth & development</topic><topic>Oryza sativa</topic><topic>Oryza sativa L</topic><topic>Phenotype</topic><topic>Plant physiology and development</topic><topic>Stress, Physiological</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kou, H.P.</creatorcontrib><creatorcontrib>Li, Y.</creatorcontrib><creatorcontrib>Song, X.X.</creatorcontrib><creatorcontrib>Ou, X.F.</creatorcontrib><creatorcontrib>Xing, S.C.</creatorcontrib><creatorcontrib>Ma, J.</creatorcontrib><creatorcontrib>Von Wettstein, D.</creatorcontrib><creatorcontrib>Liu, B.</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Nucleic Acids Abstracts</collection><jtitle>Journal of plant physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kou, H.P.</au><au>Li, Y.</au><au>Song, X.X.</au><au>Ou, X.F.</au><au>Xing, S.C.</au><au>Ma, J.</au><au>Von Wettstein, D.</au><au>Liu, B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice ( Oryza sativa L.)</atitle><jtitle>Journal of plant physiology</jtitle><addtitle>J Plant Physiol</addtitle><date>2011-09-15</date><risdate>2011</risdate><volume>168</volume><issue>14</issue><spage>1685</spage><epage>1693</epage><pages>1685-1693</pages><issn>0176-1617</issn><eissn>1618-1328</eissn><coden>JPPHEY</coden><abstract>Cytosine methylation is responsive to various biotic- and abiotic-stresses, which may produce heritable epialleles. Nitrogen (N)-deficiency is an abiotic stress being repeatedly experienced by plants. To address possible epigenetic consequences of N-deficiency-stress, we investigated the stability of cytosine methylation in rice (
Oryza sativa L.) subsequent to a chronic (a whole-generation) N-deficiency at two levels, moderate (20
mg/L) and severe (10
mg/L), under hydroponic culture. MSAP analysis revealed that locus-specific methylation alteration occurred in leaf-tissue of the stressed plants (S
0) experiencing either level of N-deficiency, which was validated by gel-blotting. Analysis on three non-stressed self-fed progenies (S
1, S
2 and S
3) by gel-blotting indicated that
ca. 50% of the altered methylation patterns in somatic cells (leaf) of the stressed S
0 plants were recaptured in S
1, which were then stably inherited to S
2 and S
3. Bisulfite sequencing of two variant MSAP loci with homology to low-copy retrotransposons on one stressed plant (S
0) and its non-stressed progenies (S
1 and S
2) showed that whereas one locus exhibited limited and non-heritable CHH methylation alteration, the other locus manifested dramatic heritable hypermethylation at nearly all cytosine sites within the assayed region. Intriguingly, when two groups of S
2 plants descended from the same N-deficiency-stressed S
0 plant were re-subjected to the stress, the group inheriting the modified methylation patterns showed enhanced tolerance to the N-deficiency-stress compared with the group bearing the original patterns. Our results thus demonstrate heritability of an acquired adaptive trait in rice, which was accompanied by epigenetic inheritance of modified cytosine methylation patterns, implicating an epigenetic basis underlying the inheritance of an acquired trait in plants.</abstract><cop>Munich</cop><pub>Elsevier GmbH</pub><pmid>21665325</pmid><doi>10.1016/j.jplph.2011.03.017</doi><tpages>9</tpages></addata></record> |
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| subjects | Abiotic stress Adaptation Adaptation, Biological - genetics Biological and medical sciences Cytosine - metabolism Cytosine methylation alteration DNA Methylation - genetics DNA, Plant - genetics Epigenesis, Genetic - genetics Epigenetic inheritance Fundamental and applied biological sciences. Psychology Genetic Loci Hydroponics Inheritance Patterns Lamarckism Nitrogen (N)-deficiency Nitrogen - deficiency Nitrogen - metabolism Oryza - genetics Oryza - growth & development Oryza sativa Oryza sativa L Phenotype Plant physiology and development Stress, Physiological |
| title | Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice ( Oryza sativa L.) |
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