Ceramides mediate positional signals in Arabidopsis thaliana protoderm differentiation
The differentiation of distinct cell types in appropriate patterns is a fundamental process in the development of multicellular organisms. In , protoderm/epidermis differentiates as a single cell layer at the outermost position. However, little is known about the molecular nature of the positional s...
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Veröffentlicht in: | Development (Cambridge) 2021-01, Vol.148 (2) |
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creator | Nagata, Kenji Ishikawa, Toshiki Kawai-Yamada, Maki Takahashi, Taku Abe, Mitsutomo |
description | The differentiation of distinct cell types in appropriate patterns is a fundamental process in the development of multicellular organisms. In
, protoderm/epidermis differentiates as a single cell layer at the outermost position. However, little is known about the molecular nature of the positional signals that achieve correct epidermal cell differentiation. Here, we propose that very-long-chain fatty acid-containing ceramides (VLCFA-Cers) mediate positional signals by stimulating the function of ARABIDOPSIS THALIANA MERISTEM LAYER1 (ATML1), a master regulator of protoderm/epidermis differentiation, during lateral root development. We show that VLCFA-Cers, which are synthesized predominantly in the outermost cells, bind to the lipid-binding domain of ATML1. Importantly, this cell type-specific protein-lipid association alters the activity of ATML1 protein and consequently restricts its expression to the protoderm/epidermis through a transcriptional feedback loop. Furthermore, establishment of a compartment, enriched with VLCFA-containing sphingolipids, at the outer lateral membrane facing the external environment may function as a determinant of protodermal cell fate. Taken together, our results indicate that VLCFA-Cers play a pivotal role in directing protoderm/epidermis differentiation by mediating positional signals to ATML1.This article has an associated 'The people behind the papers' interview. |
doi_str_mv | 10.1242/dev.194969 |
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, protoderm/epidermis differentiates as a single cell layer at the outermost position. However, little is known about the molecular nature of the positional signals that achieve correct epidermal cell differentiation. Here, we propose that very-long-chain fatty acid-containing ceramides (VLCFA-Cers) mediate positional signals by stimulating the function of ARABIDOPSIS THALIANA MERISTEM LAYER1 (ATML1), a master regulator of protoderm/epidermis differentiation, during lateral root development. We show that VLCFA-Cers, which are synthesized predominantly in the outermost cells, bind to the lipid-binding domain of ATML1. Importantly, this cell type-specific protein-lipid association alters the activity of ATML1 protein and consequently restricts its expression to the protoderm/epidermis through a transcriptional feedback loop. Furthermore, establishment of a compartment, enriched with VLCFA-containing sphingolipids, at the outer lateral membrane facing the external environment may function as a determinant of protodermal cell fate. Taken together, our results indicate that VLCFA-Cers play a pivotal role in directing protoderm/epidermis differentiation by mediating positional signals to ATML1.This article has an associated 'The people behind the papers' interview.</description><identifier>ISSN: 0950-1991</identifier><identifier>EISSN: 1477-9129</identifier><identifier>DOI: 10.1242/dev.194969</identifier><identifier>PMID: 33495212</identifier><language>eng</language><publisher>England</publisher><subject>Arabidopsis - cytology ; Arabidopsis - genetics ; Arabidopsis Proteins - chemistry ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Cell Differentiation - genetics ; Cell Lineage ; Cell Membrane - metabolism ; Ceramides - metabolism ; Gene Expression Regulation, Developmental ; Gene Expression Regulation, Plant ; Green Fluorescent Proteins - metabolism ; Ligands ; Models, Biological ; Plant Epidermis - cytology ; Plant Epidermis - genetics ; Plant Roots - embryology ; Plant Roots - metabolism ; Protein Domains ; Protein Stability ; Sphingolipids - metabolism</subject><ispartof>Development (Cambridge), 2021-01, Vol.148 (2)</ispartof><rights>2021. Published by The Company of Biologists Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c389t-b80afe7ae02072f97a4423d8417cd2f83d957cf9d0756fa6b84a4b5a8c86ef403</citedby><cites>FETCH-LOGICAL-c389t-b80afe7ae02072f97a4423d8417cd2f83d957cf9d0756fa6b84a4b5a8c86ef403</cites><orcidid>0000-0002-8423-1716</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,3678,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33495212$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nagata, Kenji</creatorcontrib><creatorcontrib>Ishikawa, Toshiki</creatorcontrib><creatorcontrib>Kawai-Yamada, Maki</creatorcontrib><creatorcontrib>Takahashi, Taku</creatorcontrib><creatorcontrib>Abe, Mitsutomo</creatorcontrib><title>Ceramides mediate positional signals in Arabidopsis thaliana protoderm differentiation</title><title>Development (Cambridge)</title><addtitle>Development</addtitle><description>The differentiation of distinct cell types in appropriate patterns is a fundamental process in the development of multicellular organisms. In
, protoderm/epidermis differentiates as a single cell layer at the outermost position. However, little is known about the molecular nature of the positional signals that achieve correct epidermal cell differentiation. Here, we propose that very-long-chain fatty acid-containing ceramides (VLCFA-Cers) mediate positional signals by stimulating the function of ARABIDOPSIS THALIANA MERISTEM LAYER1 (ATML1), a master regulator of protoderm/epidermis differentiation, during lateral root development. We show that VLCFA-Cers, which are synthesized predominantly in the outermost cells, bind to the lipid-binding domain of ATML1. Importantly, this cell type-specific protein-lipid association alters the activity of ATML1 protein and consequently restricts its expression to the protoderm/epidermis through a transcriptional feedback loop. Furthermore, establishment of a compartment, enriched with VLCFA-containing sphingolipids, at the outer lateral membrane facing the external environment may function as a determinant of protodermal cell fate. Taken together, our results indicate that VLCFA-Cers play a pivotal role in directing protoderm/epidermis differentiation by mediating positional signals to ATML1.This article has an associated 'The people behind the papers' interview.</description><subject>Arabidopsis - cytology</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis Proteins - chemistry</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Cell Differentiation - genetics</subject><subject>Cell Lineage</subject><subject>Cell Membrane - metabolism</subject><subject>Ceramides - metabolism</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Expression Regulation, Plant</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>Ligands</subject><subject>Models, Biological</subject><subject>Plant Epidermis - cytology</subject><subject>Plant Epidermis - genetics</subject><subject>Plant Roots - embryology</subject><subject>Plant Roots - metabolism</subject><subject>Protein Domains</subject><subject>Protein Stability</subject><subject>Sphingolipids - metabolism</subject><issn>0950-1991</issn><issn>1477-9129</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo9kEtLAzEUhYMotlY3_gDJUoSpec0kWUrxBQU36na4M7nRSOdhMhX890ZaXZ3Ndw6Hj5BzzpZcKHHt8GvJrbKVPSBzrrQuLBf2kMyZLVnBreUzcpLSB2NMVlofk5mUypaCizl5XWGELjhMtEMXYEI6DilMYehhQ1N4y5Fo6OlNhCa4YUwh0ekdNgF6oGMcpsFh7KgL3mPEfsoTuXtKjnwu4tk-F-Tl7vZ59VCsn-4fVzfropXGTkVjGHjUgEwwLbzVoJSQziiuWye8kc6WuvXWMV1WHqrGKFBNCaY1FXrF5IJc7nbzk88tpqnuQmpxs4Eeh22qhTKcM1NVKqNXO7SNQ0oRfT3G0EH8rjmrfz3W2WO985jhi_3utsle_tE_cfIHLXlvjA</recordid><startdate>20210125</startdate><enddate>20210125</enddate><creator>Nagata, Kenji</creator><creator>Ishikawa, Toshiki</creator><creator>Kawai-Yamada, Maki</creator><creator>Takahashi, Taku</creator><creator>Abe, Mitsutomo</creator><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><orcidid>https://orcid.org/0000-0002-8423-1716</orcidid></search><sort><creationdate>20210125</creationdate><title>Ceramides mediate positional signals in Arabidopsis thaliana protoderm differentiation</title><author>Nagata, Kenji ; Ishikawa, Toshiki ; Kawai-Yamada, Maki ; Takahashi, Taku ; Abe, Mitsutomo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c389t-b80afe7ae02072f97a4423d8417cd2f83d957cf9d0756fa6b84a4b5a8c86ef403</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Arabidopsis - cytology</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis Proteins - chemistry</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Cell Differentiation - genetics</topic><topic>Cell Lineage</topic><topic>Cell Membrane - metabolism</topic><topic>Ceramides - metabolism</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Gene Expression Regulation, Plant</topic><topic>Green Fluorescent Proteins - metabolism</topic><topic>Ligands</topic><topic>Models, Biological</topic><topic>Plant Epidermis - cytology</topic><topic>Plant Epidermis - genetics</topic><topic>Plant Roots - embryology</topic><topic>Plant Roots - metabolism</topic><topic>Protein Domains</topic><topic>Protein Stability</topic><topic>Sphingolipids - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nagata, Kenji</creatorcontrib><creatorcontrib>Ishikawa, Toshiki</creatorcontrib><creatorcontrib>Kawai-Yamada, Maki</creatorcontrib><creatorcontrib>Takahashi, Taku</creatorcontrib><creatorcontrib>Abe, Mitsutomo</creatorcontrib><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><jtitle>Development (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nagata, Kenji</au><au>Ishikawa, Toshiki</au><au>Kawai-Yamada, Maki</au><au>Takahashi, Taku</au><au>Abe, Mitsutomo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ceramides mediate positional signals in Arabidopsis thaliana protoderm differentiation</atitle><jtitle>Development (Cambridge)</jtitle><addtitle>Development</addtitle><date>2021-01-25</date><risdate>2021</risdate><volume>148</volume><issue>2</issue><issn>0950-1991</issn><eissn>1477-9129</eissn><abstract>The differentiation of distinct cell types in appropriate patterns is a fundamental process in the development of multicellular organisms. 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, protoderm/epidermis differentiates as a single cell layer at the outermost position. However, little is known about the molecular nature of the positional signals that achieve correct epidermal cell differentiation. Here, we propose that very-long-chain fatty acid-containing ceramides (VLCFA-Cers) mediate positional signals by stimulating the function of ARABIDOPSIS THALIANA MERISTEM LAYER1 (ATML1), a master regulator of protoderm/epidermis differentiation, during lateral root development. We show that VLCFA-Cers, which are synthesized predominantly in the outermost cells, bind to the lipid-binding domain of ATML1. Importantly, this cell type-specific protein-lipid association alters the activity of ATML1 protein and consequently restricts its expression to the protoderm/epidermis through a transcriptional feedback loop. Furthermore, establishment of a compartment, enriched with VLCFA-containing sphingolipids, at the outer lateral membrane facing the external environment may function as a determinant of protodermal cell fate. Taken together, our results indicate that VLCFA-Cers play a pivotal role in directing protoderm/epidermis differentiation by mediating positional signals to ATML1.This article has an associated 'The people behind the papers' interview.</abstract><cop>England</cop><pmid>33495212</pmid><doi>10.1242/dev.194969</doi><orcidid>https://orcid.org/0000-0002-8423-1716</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis - cytology Arabidopsis - genetics Arabidopsis Proteins - chemistry Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Cell Differentiation - genetics Cell Lineage Cell Membrane - metabolism Ceramides - metabolism Gene Expression Regulation, Developmental Gene Expression Regulation, Plant Green Fluorescent Proteins - metabolism Ligands Models, Biological Plant Epidermis - cytology Plant Epidermis - genetics Plant Roots - embryology Plant Roots - metabolism Protein Domains Protein Stability Sphingolipids - metabolism |
title | Ceramides mediate positional signals in Arabidopsis thaliana protoderm differentiation |
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