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MSI1 and HDA6 function interdependently to control flowering time via chromatin modifications
SUMMARY MULTICOPY SUPPRESSOR OF IRA1 (MSI1) is a conserved subunit of Polycomb Repressive Complex 2 (PRC2), which mediates gene silencing by histone H3 lysine 27 trimethylation (H3K27Me3). Here, we demonstrated that MSI1 interacts with the RPD3‐like histone deacetylase HDA6 both in vitro and in vivo...
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Published in: | The Plant journal : for cell and molecular biology 2022-02, Vol.109 (4), p.831-843 |
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creator | Xu, Yingchao Li, Qing Yuan, Lianyu Huang, Yisui Hung, Fu‐Yu Wu, Keqiang Yang, Songguang |
description | SUMMARY
MULTICOPY SUPPRESSOR OF IRA1 (MSI1) is a conserved subunit of Polycomb Repressive Complex 2 (PRC2), which mediates gene silencing by histone H3 lysine 27 trimethylation (H3K27Me3). Here, we demonstrated that MSI1 interacts with the RPD3‐like histone deacetylase HDA6 both in vitro and in vivo. MSI1 and HDA6 are involved in flowering and repress the expression of FLC, MAF4, and MAF5 by removing H3K9 acetylation but adding H3K27Me3. Chromatin immunoprecipitation analysis showed that HDA6 and MSI1 interdependently bind to the chromatin of FLC, MAF4, and MAF5. Furthermore, H3K9 deacetylation mediated by HDA6 is dependent on MSI1, while H3K27Me3 mediated by PRC2 containing MSI1 is also dependent on HDA6. Taken together, these data indicate that MSI1 and HDA6 act interdependently to repress the expression of FLC, MAF4, and MAF5 through histone modifications. Our findings reveal that the HDA6–MSI1 module mediates the interaction between histone H3 deacetylation and H3K27Me3 to repress gene expression involved in flowering time control.
Significance Statement
MSI1, a conserved subunit of Polycomb Repressive Complex 2 (PRC2), interacts with the RPD3‐like histone deacetylase HDA6 to repress the expression of FLC, MAF4, and MAF5 through decreasing histone H3 acetylation but increasing H3K27 trimethylation. The MSI1–HDA6 module acts as a bridge between the histone deacetylase complex and PRC2 to mediate the crosstalk between histone H3 deacetylation and H3K27 trimethylation involved in flowering via repressing FLC, MAF4, and MAF5 in Arabidopsis thaliana. |
doi_str_mv | 10.1111/tpj.15596 |
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MULTICOPY SUPPRESSOR OF IRA1 (MSI1) is a conserved subunit of Polycomb Repressive Complex 2 (PRC2), which mediates gene silencing by histone H3 lysine 27 trimethylation (H3K27Me3). Here, we demonstrated that MSI1 interacts with the RPD3‐like histone deacetylase HDA6 both in vitro and in vivo. MSI1 and HDA6 are involved in flowering and repress the expression of FLC, MAF4, and MAF5 by removing H3K9 acetylation but adding H3K27Me3. Chromatin immunoprecipitation analysis showed that HDA6 and MSI1 interdependently bind to the chromatin of FLC, MAF4, and MAF5. Furthermore, H3K9 deacetylation mediated by HDA6 is dependent on MSI1, while H3K27Me3 mediated by PRC2 containing MSI1 is also dependent on HDA6. Taken together, these data indicate that MSI1 and HDA6 act interdependently to repress the expression of FLC, MAF4, and MAF5 through histone modifications. Our findings reveal that the HDA6–MSI1 module mediates the interaction between histone H3 deacetylation and H3K27Me3 to repress gene expression involved in flowering time control.
Significance Statement
MSI1, a conserved subunit of Polycomb Repressive Complex 2 (PRC2), interacts with the RPD3‐like histone deacetylase HDA6 to repress the expression of FLC, MAF4, and MAF5 through decreasing histone H3 acetylation but increasing H3K27 trimethylation. The MSI1–HDA6 module acts as a bridge between the histone deacetylase complex and PRC2 to mediate the crosstalk between histone H3 deacetylation and H3K27 trimethylation involved in flowering via repressing FLC, MAF4, and MAF5 in Arabidopsis thaliana.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.15596</identifier><identifier>PMID: 34807487</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Acetylation ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Chromatin ; Chromatin - metabolism ; Chromatin Immunoprecipitation ; Deacetylation ; Flowering ; FLOWERING LOCUS C ; Flowers - genetics ; Flowers - metabolism ; Gene expression ; Gene Expression Regulation, Plant ; Gene Silencing ; Histone deacetylase ; HISTONE DEACETYLASE 6 ; Histone Deacetylases - genetics ; Histone Deacetylases - metabolism ; Histone H3 ; Histones ; Histones - metabolism ; Immunoprecipitation ; Lysine ; MADS AFFECTING FLOWERING 4 ; MADS AFFECTING FLOWERING 5 ; MADS Domain Proteins - metabolism ; Msi1 protein ; MULTICOPY SUPRESSOR OF IRA1 ; Polycomb group proteins ; Polycomb Repressive Complex 2 - genetics ; Polycomb Repressive Complex 2 - metabolism ; Repressor Proteins - metabolism</subject><ispartof>The Plant journal : for cell and molecular biology, 2022-02, Vol.109 (4), p.831-843</ispartof><rights>2021 Society for Experimental Biology and John Wiley & Sons Ltd</rights><rights>2021 Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>Copyright © 2022 John Wiley & Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3886-62ffc39932e3e1f6378922f6e96f1937f417d4e059f68134a55a8d857783d6873</citedby><cites>FETCH-LOGICAL-c3886-62ffc39932e3e1f6378922f6e96f1937f417d4e059f68134a55a8d857783d6873</cites><orcidid>0000-0001-5448-1872 ; 0000-0002-2077-7955 ; 0000-0002-5791-3594 ; 0000-0002-1875-9942</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34807487$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Xu, Yingchao</creatorcontrib><creatorcontrib>Li, Qing</creatorcontrib><creatorcontrib>Yuan, Lianyu</creatorcontrib><creatorcontrib>Huang, Yisui</creatorcontrib><creatorcontrib>Hung, Fu‐Yu</creatorcontrib><creatorcontrib>Wu, Keqiang</creatorcontrib><creatorcontrib>Yang, Songguang</creatorcontrib><title>MSI1 and HDA6 function interdependently to control flowering time via chromatin modifications</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY
MULTICOPY SUPPRESSOR OF IRA1 (MSI1) is a conserved subunit of Polycomb Repressive Complex 2 (PRC2), which mediates gene silencing by histone H3 lysine 27 trimethylation (H3K27Me3). Here, we demonstrated that MSI1 interacts with the RPD3‐like histone deacetylase HDA6 both in vitro and in vivo. MSI1 and HDA6 are involved in flowering and repress the expression of FLC, MAF4, and MAF5 by removing H3K9 acetylation but adding H3K27Me3. Chromatin immunoprecipitation analysis showed that HDA6 and MSI1 interdependently bind to the chromatin of FLC, MAF4, and MAF5. Furthermore, H3K9 deacetylation mediated by HDA6 is dependent on MSI1, while H3K27Me3 mediated by PRC2 containing MSI1 is also dependent on HDA6. Taken together, these data indicate that MSI1 and HDA6 act interdependently to repress the expression of FLC, MAF4, and MAF5 through histone modifications. Our findings reveal that the HDA6–MSI1 module mediates the interaction between histone H3 deacetylation and H3K27Me3 to repress gene expression involved in flowering time control.
Significance Statement
MSI1, a conserved subunit of Polycomb Repressive Complex 2 (PRC2), interacts with the RPD3‐like histone deacetylase HDA6 to repress the expression of FLC, MAF4, and MAF5 through decreasing histone H3 acetylation but increasing H3K27 trimethylation. The MSI1–HDA6 module acts as a bridge between the histone deacetylase complex and PRC2 to mediate the crosstalk between histone H3 deacetylation and H3K27 trimethylation involved in flowering via repressing FLC, MAF4, and MAF5 in Arabidopsis thaliana.</description><subject>Acetylation</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Chromatin</subject><subject>Chromatin - metabolism</subject><subject>Chromatin Immunoprecipitation</subject><subject>Deacetylation</subject><subject>Flowering</subject><subject>FLOWERING LOCUS C</subject><subject>Flowers - genetics</subject><subject>Flowers - metabolism</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Silencing</subject><subject>Histone deacetylase</subject><subject>HISTONE DEACETYLASE 6</subject><subject>Histone Deacetylases - genetics</subject><subject>Histone Deacetylases - metabolism</subject><subject>Histone H3</subject><subject>Histones</subject><subject>Histones - metabolism</subject><subject>Immunoprecipitation</subject><subject>Lysine</subject><subject>MADS AFFECTING FLOWERING 4</subject><subject>MADS AFFECTING FLOWERING 5</subject><subject>MADS Domain Proteins - metabolism</subject><subject>Msi1 protein</subject><subject>MULTICOPY SUPRESSOR OF IRA1</subject><subject>Polycomb group proteins</subject><subject>Polycomb Repressive Complex 2 - genetics</subject><subject>Polycomb Repressive Complex 2 - metabolism</subject><subject>Repressor Proteins - metabolism</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp10M1L5DAYx_EgLjq6HvwHJOBFD9W8tEl6FF_WEUVhXdiLlNg-0QxtMiapMv_9Zhz1sGAuuXz48vBDaJeSI5rfcZrPjmhV1WINTSgXVcEp_7uOJqQWpJAlZZtoK8YZIVRyUW6gTV4qIkslJ-jh5veUYu06fHl2IrAZXZusd9i6BKGDObgOXOoXOHncepeC77Hp_RsE655wsgPgV6tx-xz8oJN1ePCdNbbVy0r8iX4Y3UfY-fi30Z-L8_vTy-L69tf09OS6aLlSohDMmJbXNWfAgRrBpaoZMwJqYWjNpSmp7EogVW2EorzUVaVVpyopFe-EknwbHay68-BfRoipGWxsoe-1Az_GhglCFCsZZ5nu_0dnfgwuX5cVJ7koK5HV4Uq1wccYwDTzYAcdFg0lzXLzJm_evG-e7d5HcXwcoPuSnyNncLwCb7aHxfel5v7uapX8B71Xibg</recordid><startdate>202202</startdate><enddate>202202</enddate><creator>Xu, Yingchao</creator><creator>Li, Qing</creator><creator>Yuan, Lianyu</creator><creator>Huang, Yisui</creator><creator>Hung, Fu‐Yu</creator><creator>Wu, Keqiang</creator><creator>Yang, Songguang</creator><general>Blackwell Publishing Ltd</general><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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-5448-1872</orcidid><orcidid>https://orcid.org/0000-0002-2077-7955</orcidid><orcidid>https://orcid.org/0000-0002-5791-3594</orcidid><orcidid>https://orcid.org/0000-0002-1875-9942</orcidid></search><sort><creationdate>202202</creationdate><title>MSI1 and HDA6 function interdependently to control flowering time via chromatin modifications</title><author>Xu, Yingchao ; Li, Qing ; Yuan, Lianyu ; Huang, Yisui ; Hung, Fu‐Yu ; Wu, Keqiang ; Yang, Songguang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3886-62ffc39932e3e1f6378922f6e96f1937f417d4e059f68134a55a8d857783d6873</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Acetylation</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>Chromatin</topic><topic>Chromatin - metabolism</topic><topic>Chromatin Immunoprecipitation</topic><topic>Deacetylation</topic><topic>Flowering</topic><topic>FLOWERING LOCUS C</topic><topic>Flowers - genetics</topic><topic>Flowers - metabolism</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene Silencing</topic><topic>Histone deacetylase</topic><topic>HISTONE DEACETYLASE 6</topic><topic>Histone Deacetylases - genetics</topic><topic>Histone Deacetylases - metabolism</topic><topic>Histone H3</topic><topic>Histones</topic><topic>Histones - metabolism</topic><topic>Immunoprecipitation</topic><topic>Lysine</topic><topic>MADS AFFECTING FLOWERING 4</topic><topic>MADS AFFECTING FLOWERING 5</topic><topic>MADS Domain Proteins - metabolism</topic><topic>Msi1 protein</topic><topic>MULTICOPY SUPRESSOR OF IRA1</topic><topic>Polycomb group proteins</topic><topic>Polycomb Repressive Complex 2 - genetics</topic><topic>Polycomb Repressive Complex 2 - metabolism</topic><topic>Repressor Proteins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xu, Yingchao</creatorcontrib><creatorcontrib>Li, Qing</creatorcontrib><creatorcontrib>Yuan, Lianyu</creatorcontrib><creatorcontrib>Huang, Yisui</creatorcontrib><creatorcontrib>Hung, Fu‐Yu</creatorcontrib><creatorcontrib>Wu, Keqiang</creatorcontrib><creatorcontrib>Yang, Songguang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xu, Yingchao</au><au>Li, Qing</au><au>Yuan, Lianyu</au><au>Huang, Yisui</au><au>Hung, Fu‐Yu</au><au>Wu, Keqiang</au><au>Yang, Songguang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>MSI1 and HDA6 function interdependently to control flowering time via chromatin modifications</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2022-02</date><risdate>2022</risdate><volume>109</volume><issue>4</issue><spage>831</spage><epage>843</epage><pages>831-843</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>SUMMARY
MULTICOPY SUPPRESSOR OF IRA1 (MSI1) is a conserved subunit of Polycomb Repressive Complex 2 (PRC2), which mediates gene silencing by histone H3 lysine 27 trimethylation (H3K27Me3). Here, we demonstrated that MSI1 interacts with the RPD3‐like histone deacetylase HDA6 both in vitro and in vivo. MSI1 and HDA6 are involved in flowering and repress the expression of FLC, MAF4, and MAF5 by removing H3K9 acetylation but adding H3K27Me3. Chromatin immunoprecipitation analysis showed that HDA6 and MSI1 interdependently bind to the chromatin of FLC, MAF4, and MAF5. Furthermore, H3K9 deacetylation mediated by HDA6 is dependent on MSI1, while H3K27Me3 mediated by PRC2 containing MSI1 is also dependent on HDA6. Taken together, these data indicate that MSI1 and HDA6 act interdependently to repress the expression of FLC, MAF4, and MAF5 through histone modifications. Our findings reveal that the HDA6–MSI1 module mediates the interaction between histone H3 deacetylation and H3K27Me3 to repress gene expression involved in flowering time control.
Significance Statement
MSI1, a conserved subunit of Polycomb Repressive Complex 2 (PRC2), interacts with the RPD3‐like histone deacetylase HDA6 to repress the expression of FLC, MAF4, and MAF5 through decreasing histone H3 acetylation but increasing H3K27 trimethylation. The MSI1–HDA6 module acts as a bridge between the histone deacetylase complex and PRC2 to mediate the crosstalk between histone H3 deacetylation and H3K27 trimethylation involved in flowering via repressing FLC, MAF4, and MAF5 in Arabidopsis thaliana.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>34807487</pmid><doi>10.1111/tpj.15596</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-5448-1872</orcidid><orcidid>https://orcid.org/0000-0002-2077-7955</orcidid><orcidid>https://orcid.org/0000-0002-5791-3594</orcidid><orcidid>https://orcid.org/0000-0002-1875-9942</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Acetylation Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana Chromatin Chromatin - metabolism Chromatin Immunoprecipitation Deacetylation Flowering FLOWERING LOCUS C Flowers - genetics Flowers - metabolism Gene expression Gene Expression Regulation, Plant Gene Silencing Histone deacetylase HISTONE DEACETYLASE 6 Histone Deacetylases - genetics Histone Deacetylases - metabolism Histone H3 Histones Histones - metabolism Immunoprecipitation Lysine MADS AFFECTING FLOWERING 4 MADS AFFECTING FLOWERING 5 MADS Domain Proteins - metabolism Msi1 protein MULTICOPY SUPRESSOR OF IRA1 Polycomb group proteins Polycomb Repressive Complex 2 - genetics Polycomb Repressive Complex 2 - metabolism Repressor Proteins - metabolism |
title | MSI1 and HDA6 function interdependently to control flowering time via chromatin modifications |
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