Sucrose-responsive osmoregulation of plant cell size by a long non-coding RNA
In plants, sugars are the key source of energy and metabolic building blocks. The systemic transport of sugars is essential for plant growth and morphogenesis. Plants evolved intricate molecular networks to effectively distribute sugars. The dynamic distribution of these osmotically active compounds...
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Veröffentlicht in: | Molecular plant 2024-11, Vol.17 (11), p.1719-1732 |
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creator | Hajný, Jakub Trávníčková, Tereza Špundová, Martina Roenspies, Michelle Rony, R.M. Imtiaz Karim Sacharowski, Sebastian Krzyszton, Michal Zalabák, David Hardtke, Christian S. Pečinka, Aleš Puchta, Holger Swiezewski, Szymon van Norman, Jaimie M. Novák, Ondřej |
description | In plants, sugars are the key source of energy and metabolic building blocks. The systemic transport of sugars is essential for plant growth and morphogenesis. Plants evolved intricate molecular networks to effectively distribute sugars. The dynamic distribution of these osmotically active compounds is a handy tool for regulating cell turgor pressure, an instructive force in developmental biology. In this study, we have investigated the molecular mechanism behind the dual role of the receptor-like kinase CANAR. We functionally characterized a long non-coding RNA, CARMA, as a negative regulator of CANAR. Sugar-responsive CARMA specifically fine-tunes CANAR expression in the phloem, the route of sugar transport. Our genetic, molecular, microscopy, and biophysical data suggest that the CARMA–CANAR module controls the shoot-to-root phloem transport of sugars, allows cells to flexibly adapt to the external osmolality by appropriate water uptake, and thus adjust the size of vascular cell types during organ growth and development. Our study identifies a nexus of plant vascular tissue formation with cell internal pressure monitoring, revealing a novel functional aspect of long non-coding RNAs in developmental biology.
This study shows that the CARMA–CANAR module acts as a novel osmoregulatory system controlling cell size in the root stele in response to external osmolality. CANAR activity regulates the shoot-to-root phloem transport of sugars, which influences internal pressure via cellular water uptake and thus cell size. |
doi_str_mv | 10.1016/j.molp.2024.09.011 |
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This study shows that the CARMA–CANAR module acts as a novel osmoregulatory system controlling cell size in the root stele in response to external osmolality. CANAR activity regulates the shoot-to-root phloem transport of sugars, which influences internal pressure via cellular water uptake and thus cell size.</description><identifier>ISSN: 1674-2052</identifier><identifier>ISSN: 1752-9867</identifier><identifier>EISSN: 1752-9867</identifier><identifier>DOI: 10.1016/j.molp.2024.09.011</identifier><identifier>PMID: 39354717</identifier><language>eng</language><publisher>England: Elsevier Inc</publisher><subject>Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; auxin ; Cell Size ; energy ; Gene Expression Regulation, Plant ; lncRNA ; microscopy ; morphogenesis ; non-coding RNA ; osmolality ; osmoregulation ; Osmoregulation - genetics ; phloem ; Phloem - cytology ; Phloem - genetics ; Phloem - metabolism ; Plant Cells - metabolism ; plant growth ; RNA, Long Noncoding - genetics ; RNA, Long Noncoding - metabolism ; Sucrose - metabolism ; sugar transport ; sugars ; turgor ; water uptake</subject><ispartof>Molecular plant, 2024-11, Vol.17 (11), p.1719-1732</ispartof><rights>2024 The Author</rights><rights>Copyright © 2024 The Author. Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c314t-8a6ddb2cf9aed8f2131b3d916e01ec9405b29f2cd0a6b969a582ac5d2d92528f3</cites><orcidid>0000-0003-2140-7195</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39354717$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hajný, Jakub</creatorcontrib><creatorcontrib>Trávníčková, Tereza</creatorcontrib><creatorcontrib>Špundová, Martina</creatorcontrib><creatorcontrib>Roenspies, Michelle</creatorcontrib><creatorcontrib>Rony, R.M. Imtiaz Karim</creatorcontrib><creatorcontrib>Sacharowski, Sebastian</creatorcontrib><creatorcontrib>Krzyszton, Michal</creatorcontrib><creatorcontrib>Zalabák, David</creatorcontrib><creatorcontrib>Hardtke, Christian S.</creatorcontrib><creatorcontrib>Pečinka, Aleš</creatorcontrib><creatorcontrib>Puchta, Holger</creatorcontrib><creatorcontrib>Swiezewski, Szymon</creatorcontrib><creatorcontrib>van Norman, Jaimie M.</creatorcontrib><creatorcontrib>Novák, Ondřej</creatorcontrib><title>Sucrose-responsive osmoregulation of plant cell size by a long non-coding RNA</title><title>Molecular plant</title><addtitle>Mol Plant</addtitle><description>In plants, sugars are the key source of energy and metabolic building blocks. The systemic transport of sugars is essential for plant growth and morphogenesis. Plants evolved intricate molecular networks to effectively distribute sugars. The dynamic distribution of these osmotically active compounds is a handy tool for regulating cell turgor pressure, an instructive force in developmental biology. In this study, we have investigated the molecular mechanism behind the dual role of the receptor-like kinase CANAR. We functionally characterized a long non-coding RNA, CARMA, as a negative regulator of CANAR. Sugar-responsive CARMA specifically fine-tunes CANAR expression in the phloem, the route of sugar transport. Our genetic, molecular, microscopy, and biophysical data suggest that the CARMA–CANAR module controls the shoot-to-root phloem transport of sugars, allows cells to flexibly adapt to the external osmolality by appropriate water uptake, and thus adjust the size of vascular cell types during organ growth and development. Our study identifies a nexus of plant vascular tissue formation with cell internal pressure monitoring, revealing a novel functional aspect of long non-coding RNAs in developmental biology.
This study shows that the CARMA–CANAR module acts as a novel osmoregulatory system controlling cell size in the root stele in response to external osmolality. CANAR activity regulates the shoot-to-root phloem transport of sugars, which influences internal pressure via cellular water uptake and thus cell size.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>auxin</subject><subject>Cell Size</subject><subject>energy</subject><subject>Gene Expression Regulation, Plant</subject><subject>lncRNA</subject><subject>microscopy</subject><subject>morphogenesis</subject><subject>non-coding RNA</subject><subject>osmolality</subject><subject>osmoregulation</subject><subject>Osmoregulation - genetics</subject><subject>phloem</subject><subject>Phloem - cytology</subject><subject>Phloem - genetics</subject><subject>Phloem - metabolism</subject><subject>Plant Cells - metabolism</subject><subject>plant growth</subject><subject>RNA, Long Noncoding - genetics</subject><subject>RNA, Long Noncoding - metabolism</subject><subject>Sucrose - metabolism</subject><subject>sugar transport</subject><subject>sugars</subject><subject>turgor</subject><subject>water uptake</subject><issn>1674-2052</issn><issn>1752-9867</issn><issn>1752-9867</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkM1O3jAQRa2KqlDKC3RReckmqceOnVhigxD9kaBIUNaWY0-QPyVxsBMk-vQk-miXFau5i3OvRoeQz8BKYKC-7soh9lPJGa9KpksG8I4cQS15oRtVH6xZ1VXBmeSH5GPOO8YUa5T4QA6FFrKqoT4i13eLSzFjkTBPcczhCWnMQ0z4sPR2DnGksaNTb8eZOux7msMfpO0ztbSP4wMd41i46MMab3-dfyLvO9tnPHm9x-T-2-Xvix_F1c33nxfnV4UTUM1FY5X3LXedtuibjoOAVngNChmg0xWTLdcdd55Z1WqlrWy4ddJzr7nkTSeOyel-d0rxccE8myHk7T07YlyyESArkFpK8QYUOIBSgq0o36ObkZywM1MKg03PBpjZjJud2Yybzbhh2qzG19KX1_2lHdD_q_xVvAJnewBXIU8Bk8ku4OjQh4RuNj6G_-2_ANX6kcQ</recordid><startdate>20241104</startdate><enddate>20241104</enddate><creator>Hajný, Jakub</creator><creator>Trávníčková, Tereza</creator><creator>Špundová, Martina</creator><creator>Roenspies, Michelle</creator><creator>Rony, R.M. Imtiaz Karim</creator><creator>Sacharowski, Sebastian</creator><creator>Krzyszton, Michal</creator><creator>Zalabák, David</creator><creator>Hardtke, Christian S.</creator><creator>Pečinka, Aleš</creator><creator>Puchta, Holger</creator><creator>Swiezewski, Szymon</creator><creator>van Norman, Jaimie M.</creator><creator>Novák, Ondřej</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</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>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0003-2140-7195</orcidid></search><sort><creationdate>20241104</creationdate><title>Sucrose-responsive osmoregulation of plant cell size by a long non-coding RNA</title><author>Hajný, Jakub ; Trávníčková, Tereza ; Špundová, Martina ; Roenspies, Michelle ; Rony, R.M. Imtiaz Karim ; Sacharowski, Sebastian ; Krzyszton, Michal ; Zalabák, David ; Hardtke, Christian S. ; Pečinka, Aleš ; Puchta, Holger ; Swiezewski, Szymon ; van Norman, Jaimie M. ; Novák, Ondřej</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c314t-8a6ddb2cf9aed8f2131b3d916e01ec9405b29f2cd0a6b969a582ac5d2d92528f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>auxin</topic><topic>Cell Size</topic><topic>energy</topic><topic>Gene Expression Regulation, Plant</topic><topic>lncRNA</topic><topic>microscopy</topic><topic>morphogenesis</topic><topic>non-coding RNA</topic><topic>osmolality</topic><topic>osmoregulation</topic><topic>Osmoregulation - genetics</topic><topic>phloem</topic><topic>Phloem - cytology</topic><topic>Phloem - genetics</topic><topic>Phloem - metabolism</topic><topic>Plant Cells - metabolism</topic><topic>plant growth</topic><topic>RNA, Long Noncoding - genetics</topic><topic>RNA, Long Noncoding - metabolism</topic><topic>Sucrose - metabolism</topic><topic>sugar transport</topic><topic>sugars</topic><topic>turgor</topic><topic>water uptake</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hajný, Jakub</creatorcontrib><creatorcontrib>Trávníčková, Tereza</creatorcontrib><creatorcontrib>Špundová, Martina</creatorcontrib><creatorcontrib>Roenspies, Michelle</creatorcontrib><creatorcontrib>Rony, R.M. Imtiaz Karim</creatorcontrib><creatorcontrib>Sacharowski, Sebastian</creatorcontrib><creatorcontrib>Krzyszton, Michal</creatorcontrib><creatorcontrib>Zalabák, David</creatorcontrib><creatorcontrib>Hardtke, Christian S.</creatorcontrib><creatorcontrib>Pečinka, Aleš</creatorcontrib><creatorcontrib>Puchta, Holger</creatorcontrib><creatorcontrib>Swiezewski, Szymon</creatorcontrib><creatorcontrib>van Norman, Jaimie M.</creatorcontrib><creatorcontrib>Novák, Ondřej</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</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>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Molecular plant</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hajný, Jakub</au><au>Trávníčková, Tereza</au><au>Špundová, Martina</au><au>Roenspies, Michelle</au><au>Rony, R.M. Imtiaz Karim</au><au>Sacharowski, Sebastian</au><au>Krzyszton, Michal</au><au>Zalabák, David</au><au>Hardtke, Christian S.</au><au>Pečinka, Aleš</au><au>Puchta, Holger</au><au>Swiezewski, Szymon</au><au>van Norman, Jaimie M.</au><au>Novák, Ondřej</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Sucrose-responsive osmoregulation of plant cell size by a long non-coding RNA</atitle><jtitle>Molecular plant</jtitle><addtitle>Mol Plant</addtitle><date>2024-11-04</date><risdate>2024</risdate><volume>17</volume><issue>11</issue><spage>1719</spage><epage>1732</epage><pages>1719-1732</pages><issn>1674-2052</issn><issn>1752-9867</issn><eissn>1752-9867</eissn><abstract>In plants, sugars are the key source of energy and metabolic building blocks. The systemic transport of sugars is essential for plant growth and morphogenesis. Plants evolved intricate molecular networks to effectively distribute sugars. The dynamic distribution of these osmotically active compounds is a handy tool for regulating cell turgor pressure, an instructive force in developmental biology. In this study, we have investigated the molecular mechanism behind the dual role of the receptor-like kinase CANAR. We functionally characterized a long non-coding RNA, CARMA, as a negative regulator of CANAR. Sugar-responsive CARMA specifically fine-tunes CANAR expression in the phloem, the route of sugar transport. Our genetic, molecular, microscopy, and biophysical data suggest that the CARMA–CANAR module controls the shoot-to-root phloem transport of sugars, allows cells to flexibly adapt to the external osmolality by appropriate water uptake, and thus adjust the size of vascular cell types during organ growth and development. Our study identifies a nexus of plant vascular tissue formation with cell internal pressure monitoring, revealing a novel functional aspect of long non-coding RNAs in developmental biology.
This study shows that the CARMA–CANAR module acts as a novel osmoregulatory system controlling cell size in the root stele in response to external osmolality. CANAR activity regulates the shoot-to-root phloem transport of sugars, which influences internal pressure via cellular water uptake and thus cell size.</abstract><cop>England</cop><pub>Elsevier Inc</pub><pmid>39354717</pmid><doi>10.1016/j.molp.2024.09.011</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-2140-7195</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism auxin Cell Size energy Gene Expression Regulation, Plant lncRNA microscopy morphogenesis non-coding RNA osmolality osmoregulation Osmoregulation - genetics phloem Phloem - cytology Phloem - genetics Phloem - metabolism Plant Cells - metabolism plant growth RNA, Long Noncoding - genetics RNA, Long Noncoding - metabolism Sucrose - metabolism sugar transport sugars turgor water uptake |
title | Sucrose-responsive osmoregulation of plant cell size by a long non-coding RNA |
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