N6-methyladenosine-mediated feedback regulation of abscisic acid perception via phase-separated ECT8 condensates in Arabidopsis
N 6 -methyladenosine (m 6 A) is the most abundant internal modification in eukaryotic mRNAs, yet how plants recognize this chemical modification to swiftly adjust developmental plasticity under environmental stresses remains unclear. Here we show that m 6 A mRNA modification and its reader protein E...
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Veröffentlicht in: | Nature plants 2024-03, Vol.10 (3), p.469-482 |
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creator | Wu, Xiaowei Su, Tingting Zhang, Songyao Zhang, Yu Wong, Chui Eng Ma, Jinqi Shao, Yanlin Hua, Changmei Shen, Lisha Yu, Hao |
description | N
6
-methyladenosine (m
6
A) is the most abundant internal modification in eukaryotic mRNAs, yet how plants recognize this chemical modification to swiftly adjust developmental plasticity under environmental stresses remains unclear. Here we show that m
6
A mRNA modification and its reader protein EVOLUTIONARILY CONSERVED C-TERMINAL REGION 8 (ECT8) act together as a key checkpoint for negative feedback regulation of abscisic acid (ABA) signalling by sequestering the m
6
A-modified ABA receptor gene
PYRABACTIN RESISTANCE 1-LIKE 7
(
PYL7
) via phase-separated ECT8 condensates in stress granules in response to ABA. This partially depletes
PYL7
mRNA from its translation in the cytoplasm, thus reducing PYL7 protein levels and compromising ABA perception. The loss of ECT8 results in defective sequestration of m
6
A-modified
PYL7
in stress granules and permits more
PYL7
transcripts for translation. This causes overactivation of ABA-responsive genes and the consequent ABA-hypersensitive phenotypes, including drought tolerance. Overall, our findings reveal that m
6
A-mediated sequestration of
PYL7
by ECT8 in stress granules negatively regulates ABA perception, thereby enabling prompt feedback regulation of ABA signalling to prevent plant cell overreaction to environmental stresses.
In response to abscisic acid, the m
6
A reader ECT8 undergoes phase separation to form cytoplasmic condensates and sequesters m
6
A-modified abscisic acid receptor
PYL7
mRNA in stress granules, which suppresses PYL7 translation for feedback regulation of abscisic acid perception. |
doi_str_mv | 10.1038/s41477-024-01638-7 |
format | Article |
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6
-methyladenosine (m
6
A) is the most abundant internal modification in eukaryotic mRNAs, yet how plants recognize this chemical modification to swiftly adjust developmental plasticity under environmental stresses remains unclear. Here we show that m
6
A mRNA modification and its reader protein EVOLUTIONARILY CONSERVED C-TERMINAL REGION 8 (ECT8) act together as a key checkpoint for negative feedback regulation of abscisic acid (ABA) signalling by sequestering the m
6
A-modified ABA receptor gene
PYRABACTIN RESISTANCE 1-LIKE 7
(
PYL7
) via phase-separated ECT8 condensates in stress granules in response to ABA. This partially depletes
PYL7
mRNA from its translation in the cytoplasm, thus reducing PYL7 protein levels and compromising ABA perception. The loss of ECT8 results in defective sequestration of m
6
A-modified
PYL7
in stress granules and permits more
PYL7
transcripts for translation. This causes overactivation of ABA-responsive genes and the consequent ABA-hypersensitive phenotypes, including drought tolerance. Overall, our findings reveal that m
6
A-mediated sequestration of
PYL7
by ECT8 in stress granules negatively regulates ABA perception, thereby enabling prompt feedback regulation of ABA signalling to prevent plant cell overreaction to environmental stresses.
In response to abscisic acid, the m
6
A reader ECT8 undergoes phase separation to form cytoplasmic condensates and sequesters m
6
A-modified abscisic acid receptor
PYL7
mRNA in stress granules, which suppresses PYL7 translation for feedback regulation of abscisic acid perception.</description><identifier>ISSN: 2055-0278</identifier><identifier>EISSN: 2055-0278</identifier><identifier>DOI: 10.1038/s41477-024-01638-7</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38/39 ; 38/71 ; 38/90 ; 45/91 ; 631/449/2661/2665 ; 631/80/86/2366 ; 82/58 ; 82/83 ; Abscisic acid ; Biomedical and Life Sciences ; Chemical modification ; Condensates ; Cytoplasm ; Developmental plasticity ; Drought resistance ; Environmental stress ; Feedback ; Granular materials ; Life Sciences ; N6-methyladenosine ; Negative feedback ; Perception ; Phase separation ; Phenotypes ; Plant Sciences ; Proteins ; Receptors ; RNA modification ; Sequestering ; Stresses ; Translation</subject><ispartof>Nature plants, 2024-03, Vol.10 (3), p.469-482</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2024. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c282t-f3c860115920e584acae45b244a243bd7c3dde6763c90a6892cd24ff272d96663</citedby><cites>FETCH-LOGICAL-c282t-f3c860115920e584acae45b244a243bd7c3dde6763c90a6892cd24ff272d96663</cites><orcidid>0000-0002-1808-6370 ; 0000-0001-5674-4023 ; 0000-0002-9778-8855</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41477-024-01638-7$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41477-024-01638-7$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27923,27924,41487,42556,51318</link.rule.ids></links><search><creatorcontrib>Wu, Xiaowei</creatorcontrib><creatorcontrib>Su, Tingting</creatorcontrib><creatorcontrib>Zhang, Songyao</creatorcontrib><creatorcontrib>Zhang, Yu</creatorcontrib><creatorcontrib>Wong, Chui Eng</creatorcontrib><creatorcontrib>Ma, Jinqi</creatorcontrib><creatorcontrib>Shao, Yanlin</creatorcontrib><creatorcontrib>Hua, Changmei</creatorcontrib><creatorcontrib>Shen, Lisha</creatorcontrib><creatorcontrib>Yu, Hao</creatorcontrib><title>N6-methyladenosine-mediated feedback regulation of abscisic acid perception via phase-separated ECT8 condensates in Arabidopsis</title><title>Nature plants</title><addtitle>Nat. Plants</addtitle><description>N
6
-methyladenosine (m
6
A) is the most abundant internal modification in eukaryotic mRNAs, yet how plants recognize this chemical modification to swiftly adjust developmental plasticity under environmental stresses remains unclear. Here we show that m
6
A mRNA modification and its reader protein EVOLUTIONARILY CONSERVED C-TERMINAL REGION 8 (ECT8) act together as a key checkpoint for negative feedback regulation of abscisic acid (ABA) signalling by sequestering the m
6
A-modified ABA receptor gene
PYRABACTIN RESISTANCE 1-LIKE 7
(
PYL7
) via phase-separated ECT8 condensates in stress granules in response to ABA. This partially depletes
PYL7
mRNA from its translation in the cytoplasm, thus reducing PYL7 protein levels and compromising ABA perception. The loss of ECT8 results in defective sequestration of m
6
A-modified
PYL7
in stress granules and permits more
PYL7
transcripts for translation. This causes overactivation of ABA-responsive genes and the consequent ABA-hypersensitive phenotypes, including drought tolerance. Overall, our findings reveal that m
6
A-mediated sequestration of
PYL7
by ECT8 in stress granules negatively regulates ABA perception, thereby enabling prompt feedback regulation of ABA signalling to prevent plant cell overreaction to environmental stresses.
In response to abscisic acid, the m
6
A reader ECT8 undergoes phase separation to form cytoplasmic condensates and sequesters m
6
A-modified abscisic acid receptor
PYL7
mRNA in stress granules, which suppresses PYL7 translation for feedback regulation of abscisic acid perception.</description><subject>38/39</subject><subject>38/71</subject><subject>38/90</subject><subject>45/91</subject><subject>631/449/2661/2665</subject><subject>631/80/86/2366</subject><subject>82/58</subject><subject>82/83</subject><subject>Abscisic acid</subject><subject>Biomedical and Life Sciences</subject><subject>Chemical modification</subject><subject>Condensates</subject><subject>Cytoplasm</subject><subject>Developmental plasticity</subject><subject>Drought resistance</subject><subject>Environmental stress</subject><subject>Feedback</subject><subject>Granular materials</subject><subject>Life Sciences</subject><subject>N6-methyladenosine</subject><subject>Negative feedback</subject><subject>Perception</subject><subject>Phase separation</subject><subject>Phenotypes</subject><subject>Plant Sciences</subject><subject>Proteins</subject><subject>Receptors</subject><subject>RNA modification</subject><subject>Sequestering</subject><subject>Stresses</subject><subject>Translation</subject><issn>2055-0278</issn><issn>2055-0278</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp9kUtrFUEQhQdRMCT5A64a3LgZ7Xf3LMMlPiDoJq6bmu6apOPc6bFrrpCVf932XkFxkVW9vnMoOF33SvC3giv_jrTQzvVc6p4Lq3zvnnVnkhvTVs4__6d_2V0SPXDOhTNGWX7W_fxs-z1u948zJFwK5QXbnDJsmNiEmEaI31jFu8MMWy4LKxODkWKmHBnEnNiKNeJ6vP3IwNZ7IOwJV6hHj-vdrWexLM2d2oJYXthVhTGnslKmi-7FBDPh5Z963n19f327-9jffPnwaXd100fp5dZPKnrLhTCD5Gi8hgiozSi1BqnVmFxUKaF1VsWBg_WDjEnqaZJOpsFaq867NyfftZbvB6Qt7DNFnGdYsBwoyEFL4Y3jvKGv_0MfyqEu7btG2UEaYbxvlDxRsRaiilNYa95DfQyCh9-xhFMsocUSjrEE10TqJKIGL3dY_1o_ofoFHsOQkQ</recordid><startdate>20240301</startdate><enddate>20240301</enddate><creator>Wu, Xiaowei</creator><creator>Su, Tingting</creator><creator>Zhang, Songyao</creator><creator>Zhang, Yu</creator><creator>Wong, Chui Eng</creator><creator>Ma, Jinqi</creator><creator>Shao, Yanlin</creator><creator>Hua, Changmei</creator><creator>Shen, Lisha</creator><creator>Yu, Hao</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7SN</scope><scope>C1K</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-1808-6370</orcidid><orcidid>https://orcid.org/0000-0001-5674-4023</orcidid><orcidid>https://orcid.org/0000-0002-9778-8855</orcidid></search><sort><creationdate>20240301</creationdate><title>N6-methyladenosine-mediated feedback regulation of abscisic acid perception via phase-separated ECT8 condensates in Arabidopsis</title><author>Wu, Xiaowei ; Su, Tingting ; Zhang, Songyao ; Zhang, Yu ; Wong, Chui Eng ; Ma, Jinqi ; Shao, Yanlin ; Hua, Changmei ; Shen, Lisha ; Yu, Hao</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c282t-f3c860115920e584acae45b244a243bd7c3dde6763c90a6892cd24ff272d96663</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>38/39</topic><topic>38/71</topic><topic>38/90</topic><topic>45/91</topic><topic>631/449/2661/2665</topic><topic>631/80/86/2366</topic><topic>82/58</topic><topic>82/83</topic><topic>Abscisic acid</topic><topic>Biomedical and Life Sciences</topic><topic>Chemical modification</topic><topic>Condensates</topic><topic>Cytoplasm</topic><topic>Developmental plasticity</topic><topic>Drought resistance</topic><topic>Environmental stress</topic><topic>Feedback</topic><topic>Granular materials</topic><topic>Life Sciences</topic><topic>N6-methyladenosine</topic><topic>Negative feedback</topic><topic>Perception</topic><topic>Phase separation</topic><topic>Phenotypes</topic><topic>Plant Sciences</topic><topic>Proteins</topic><topic>Receptors</topic><topic>RNA modification</topic><topic>Sequestering</topic><topic>Stresses</topic><topic>Translation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wu, Xiaowei</creatorcontrib><creatorcontrib>Su, Tingting</creatorcontrib><creatorcontrib>Zhang, Songyao</creatorcontrib><creatorcontrib>Zhang, Yu</creatorcontrib><creatorcontrib>Wong, Chui Eng</creatorcontrib><creatorcontrib>Ma, Jinqi</creatorcontrib><creatorcontrib>Shao, Yanlin</creatorcontrib><creatorcontrib>Hua, Changmei</creatorcontrib><creatorcontrib>Shen, Lisha</creatorcontrib><creatorcontrib>Yu, Hao</creatorcontrib><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>MEDLINE - Academic</collection><jtitle>Nature plants</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wu, Xiaowei</au><au>Su, Tingting</au><au>Zhang, Songyao</au><au>Zhang, Yu</au><au>Wong, Chui Eng</au><au>Ma, Jinqi</au><au>Shao, Yanlin</au><au>Hua, Changmei</au><au>Shen, Lisha</au><au>Yu, Hao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>N6-methyladenosine-mediated feedback regulation of abscisic acid perception via phase-separated ECT8 condensates in Arabidopsis</atitle><jtitle>Nature plants</jtitle><stitle>Nat. Plants</stitle><date>2024-03-01</date><risdate>2024</risdate><volume>10</volume><issue>3</issue><spage>469</spage><epage>482</epage><pages>469-482</pages><issn>2055-0278</issn><eissn>2055-0278</eissn><abstract>N
6
-methyladenosine (m
6
A) is the most abundant internal modification in eukaryotic mRNAs, yet how plants recognize this chemical modification to swiftly adjust developmental plasticity under environmental stresses remains unclear. Here we show that m
6
A mRNA modification and its reader protein EVOLUTIONARILY CONSERVED C-TERMINAL REGION 8 (ECT8) act together as a key checkpoint for negative feedback regulation of abscisic acid (ABA) signalling by sequestering the m
6
A-modified ABA receptor gene
PYRABACTIN RESISTANCE 1-LIKE 7
(
PYL7
) via phase-separated ECT8 condensates in stress granules in response to ABA. This partially depletes
PYL7
mRNA from its translation in the cytoplasm, thus reducing PYL7 protein levels and compromising ABA perception. The loss of ECT8 results in defective sequestration of m
6
A-modified
PYL7
in stress granules and permits more
PYL7
transcripts for translation. This causes overactivation of ABA-responsive genes and the consequent ABA-hypersensitive phenotypes, including drought tolerance. Overall, our findings reveal that m
6
A-mediated sequestration of
PYL7
by ECT8 in stress granules negatively regulates ABA perception, thereby enabling prompt feedback regulation of ABA signalling to prevent plant cell overreaction to environmental stresses.
In response to abscisic acid, the m
6
A reader ECT8 undergoes phase separation to form cytoplasmic condensates and sequesters m
6
A-modified abscisic acid receptor
PYL7
mRNA in stress granules, which suppresses PYL7 translation for feedback regulation of abscisic acid perception.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><doi>10.1038/s41477-024-01638-7</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-1808-6370</orcidid><orcidid>https://orcid.org/0000-0001-5674-4023</orcidid><orcidid>https://orcid.org/0000-0002-9778-8855</orcidid></addata></record> |
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subjects | 38/39 38/71 38/90 45/91 631/449/2661/2665 631/80/86/2366 82/58 82/83 Abscisic acid Biomedical and Life Sciences Chemical modification Condensates Cytoplasm Developmental plasticity Drought resistance Environmental stress Feedback Granular materials Life Sciences N6-methyladenosine Negative feedback Perception Phase separation Phenotypes Plant Sciences Proteins Receptors RNA modification Sequestering Stresses Translation |
title | N6-methyladenosine-mediated feedback regulation of abscisic acid perception via phase-separated ECT8 condensates in Arabidopsis |
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