TOR represses stress responses through global regulation of H3K27 trimethylation in plants
Abstract Target of rapamycin (TOR) functions as a central sensory hub linking a wide range of external stimuli to gene expression. The mechanisms underlying stimulus-specific transcriptional reprogramming by TOR remain elusive. Here, we describe an in silico analysis in Arabidopsis demonstrating tha...
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| Veröffentlicht in: | Journal of experimental botany 2023-03, Vol.74 (5), p.1420-1431 |
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| container_title | Journal of experimental botany |
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| creator | Dong, Yihan Uslu, Veli V Berr, Alexandre Singh, Gaurav Papdi, Csaba Steffens, Victor A Heitz, Thierry Ryabova, Lyubov A |
| description | Abstract
Target of rapamycin (TOR) functions as a central sensory hub linking a wide range of external stimuli to gene expression. The mechanisms underlying stimulus-specific transcriptional reprogramming by TOR remain elusive. Here, we describe an in silico analysis in Arabidopsis demonstrating that TOR-repressed genes are associated with either bistable or silent chromatin states. Both states regulated by the TOR signaling pathway are associated with a high level of histone H3K27 trimethylation (H3K27me3) deposited by CURLY LEAF in a specific context with LIKE HETEROCHROMATIN PROTEIN1. The combination of the two epigenetic histone modifications H3K4me3 and H3K27me3 implicates a bistable feature that alternates between an ‘on’ and an ‘off’ state, allowing rapid transcriptional changes upon external stimuli. The chromatin remodeler SWI2/SNF2 ATPase BRAHMA activates TOR-repressed genes only at bistable chromatin domains to rapidly induce biotic stress responses. Here, we demonstrate both in silico and in vivo that TOR represses transcriptional stress responses through global maintenance of H3K27me3.
TOR regulates gene expression upon environmental stimuli via two types of chromatin, namely the repressive chromatin marked by H3K27me3 and the bistable chromatin marked by both H3K27me3 and H3K4me3. |
| doi_str_mv | 10.1093/jxb/erac486 |
| format | Article |
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Target of rapamycin (TOR) functions as a central sensory hub linking a wide range of external stimuli to gene expression. The mechanisms underlying stimulus-specific transcriptional reprogramming by TOR remain elusive. Here, we describe an in silico analysis in Arabidopsis demonstrating that TOR-repressed genes are associated with either bistable or silent chromatin states. Both states regulated by the TOR signaling pathway are associated with a high level of histone H3K27 trimethylation (H3K27me3) deposited by CURLY LEAF in a specific context with LIKE HETEROCHROMATIN PROTEIN1. The combination of the two epigenetic histone modifications H3K4me3 and H3K27me3 implicates a bistable feature that alternates between an ‘on’ and an ‘off’ state, allowing rapid transcriptional changes upon external stimuli. The chromatin remodeler SWI2/SNF2 ATPase BRAHMA activates TOR-repressed genes only at bistable chromatin domains to rapidly induce biotic stress responses. Here, we demonstrate both in silico and in vivo that TOR represses transcriptional stress responses through global maintenance of H3K27me3.
TOR regulates gene expression upon environmental stimuli via two types of chromatin, namely the repressive chromatin marked by H3K27me3 and the bistable chromatin marked by both H3K27me3 and H3K4me3.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/erac486</identifier><identifier>PMID: 36515098</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Chromatin - genetics ; Chromatin - metabolism ; Chromatin Assembly and Disassembly ; Gene Expression Regulation, Plant ; Histones - genetics ; Histones - metabolism ; Life Sciences ; Phosphatidylinositol 3-Kinases - genetics ; Vegetal Biology</subject><ispartof>Journal of experimental botany, 2023-03, Vol.74 (5), p.1420-1431</ispartof><rights>The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com 2022</rights><rights>The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c391t-edac6bf6c570a4dde059a7135b9485621d296ba1e82ca6b5b37bf049bdeba81f3</citedby><cites>FETCH-LOGICAL-c391t-edac6bf6c570a4dde059a7135b9485621d296ba1e82ca6b5b37bf049bdeba81f3</cites><orcidid>0000-0001-6238-8264 ; 0000-0002-3238-4681 ; 0000-0003-1989-203X ; 0000-0002-1381-9053</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,1578,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36515098$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04040214$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Dong, Yihan</creatorcontrib><creatorcontrib>Uslu, Veli V</creatorcontrib><creatorcontrib>Berr, Alexandre</creatorcontrib><creatorcontrib>Singh, Gaurav</creatorcontrib><creatorcontrib>Papdi, Csaba</creatorcontrib><creatorcontrib>Steffens, Victor A</creatorcontrib><creatorcontrib>Heitz, Thierry</creatorcontrib><creatorcontrib>Ryabova, Lyubov A</creatorcontrib><title>TOR represses stress responses through global regulation of H3K27 trimethylation in plants</title><title>Journal of experimental botany</title><addtitle>J Exp Bot</addtitle><description>Abstract
Target of rapamycin (TOR) functions as a central sensory hub linking a wide range of external stimuli to gene expression. The mechanisms underlying stimulus-specific transcriptional reprogramming by TOR remain elusive. Here, we describe an in silico analysis in Arabidopsis demonstrating that TOR-repressed genes are associated with either bistable or silent chromatin states. Both states regulated by the TOR signaling pathway are associated with a high level of histone H3K27 trimethylation (H3K27me3) deposited by CURLY LEAF in a specific context with LIKE HETEROCHROMATIN PROTEIN1. The combination of the two epigenetic histone modifications H3K4me3 and H3K27me3 implicates a bistable feature that alternates between an ‘on’ and an ‘off’ state, allowing rapid transcriptional changes upon external stimuli. The chromatin remodeler SWI2/SNF2 ATPase BRAHMA activates TOR-repressed genes only at bistable chromatin domains to rapidly induce biotic stress responses. Here, we demonstrate both in silico and in vivo that TOR represses transcriptional stress responses through global maintenance of H3K27me3.
TOR regulates gene expression upon environmental stimuli via two types of chromatin, namely the repressive chromatin marked by H3K27me3 and the bistable chromatin marked by both H3K27me3 and H3K4me3.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Chromatin - genetics</subject><subject>Chromatin - metabolism</subject><subject>Chromatin Assembly and Disassembly</subject><subject>Gene Expression Regulation, Plant</subject><subject>Histones - genetics</subject><subject>Histones - metabolism</subject><subject>Life Sciences</subject><subject>Phosphatidylinositol 3-Kinases - genetics</subject><subject>Vegetal Biology</subject><issn>0022-0957</issn><issn>1460-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kM9LwzAUx4Mobk5P3qUnUaTuJU364ziGOnEwkHnxEpI2XTu6pSatuP_elNYd5R3e4_s-fPnyRegawyOGJJhuf-RUGZHSODxBY0xD8AkN8CkaAxDiQ8KiEbqwdgsADBg7R6MgZJhBEo_R53r17hlVG2Wtsp5tusMJttb7TmgKo9tN4W0qLUXlHpu2Ek2p957OvUXwRiKvMeVONcVh0Mu9V1di39hLdJaLyqqrYU_Qx_PTer7wl6uX1_ls6adBghtfZSINZR6mLAJBs0wBS0SEAyYTGrOQ4IwkoRRYxSQVoWQyiGQONJGZkiLGeTBB971vISpeuzDCHLgWJV_MlrzTgLohmH4Tx971bG30V6tsw3elTVXlAivdWk4iRhlQGlOHPvRoarS1RuVHbwy8K5674vlQvKNvBuNW7lR2ZP-adsBtD-i2_tfpF_NpjR8</recordid><startdate>20230313</startdate><enddate>20230313</enddate><creator>Dong, Yihan</creator><creator>Uslu, Veli V</creator><creator>Berr, Alexandre</creator><creator>Singh, Gaurav</creator><creator>Papdi, Csaba</creator><creator>Steffens, Victor A</creator><creator>Heitz, Thierry</creator><creator>Ryabova, Lyubov A</creator><general>Oxford University Press</general><general>Oxford University Press (OUP)</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>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0001-6238-8264</orcidid><orcidid>https://orcid.org/0000-0002-3238-4681</orcidid><orcidid>https://orcid.org/0000-0003-1989-203X</orcidid><orcidid>https://orcid.org/0000-0002-1381-9053</orcidid></search><sort><creationdate>20230313</creationdate><title>TOR represses stress responses through global regulation of H3K27 trimethylation in plants</title><author>Dong, Yihan ; 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Target of rapamycin (TOR) functions as a central sensory hub linking a wide range of external stimuli to gene expression. The mechanisms underlying stimulus-specific transcriptional reprogramming by TOR remain elusive. Here, we describe an in silico analysis in Arabidopsis demonstrating that TOR-repressed genes are associated with either bistable or silent chromatin states. Both states regulated by the TOR signaling pathway are associated with a high level of histone H3K27 trimethylation (H3K27me3) deposited by CURLY LEAF in a specific context with LIKE HETEROCHROMATIN PROTEIN1. The combination of the two epigenetic histone modifications H3K4me3 and H3K27me3 implicates a bistable feature that alternates between an ‘on’ and an ‘off’ state, allowing rapid transcriptional changes upon external stimuli. The chromatin remodeler SWI2/SNF2 ATPase BRAHMA activates TOR-repressed genes only at bistable chromatin domains to rapidly induce biotic stress responses. Here, we demonstrate both in silico and in vivo that TOR represses transcriptional stress responses through global maintenance of H3K27me3.
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| source | Oxford University Press Journals All Titles (1996-Current); MEDLINE; EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection |
| subjects | Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Chromatin - genetics Chromatin - metabolism Chromatin Assembly and Disassembly Gene Expression Regulation, Plant Histones - genetics Histones - metabolism Life Sciences Phosphatidylinositol 3-Kinases - genetics Vegetal Biology |
| title | TOR represses stress responses through global regulation of H3K27 trimethylation in plants |
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