Antagonistic CLE peptide pathways shape root meristem tissue patterning
Secreted CLAVATA3/EMBRYO SURROUNDING REGION (CLE) peptide ligands dimension the stem cell niche of Arabidopsis shoot meristems by signalling through redundant and cross-compensating CLAVATA1 (CLV1)-type receptor kinases. In the root meristem, the CLV1 homologues BARELY ANY MERISTEM 1 (BAM1) and BAM2...
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| Veröffentlicht in: | Nature plants 2024-12, Vol.10 (12), p.1900-1908 |
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| creator | Zhang, Hang Wang, Qian Blanco-Touriñán, Noel Hardtke, Christian S. |
| description | Secreted CLAVATA3/EMBRYO SURROUNDING REGION (CLE) peptide ligands dimension the stem cell niche of
Arabidopsis
shoot meristems by signalling through redundant and cross-compensating CLAVATA1 (CLV1)-type receptor kinases. In the root meristem, the CLV1 homologues BARELY ANY MERISTEM 1 (BAM1) and BAM2 drive CLE13/16-mediated formative divisions that produce the ground tissue layers. Here we report that BAM1/2 are also required to initiate the vascular phloem lineage and that cross-compensation between CLV1-type receptors as observed in the shoot does not operate similarly in the root. Rather, we find that BAM3-mediated CLE45 signalling antagonizes BAM1/2-mediated CLE11/12/13 signalling in the phloem initials but not in the ground tissue. We further observe spatiotemporally contrasting CLE signalling requirements for phloem initiation and differentiation, which are shaped by the SHORT ROOT (SHR) pathway. Our findings thus suggest an intricate quantitative interplay between distinct and antagonistic CLE signalling pathways that organizes tissue layer formation in the
Arabidopsis
root meristem.
The activity of distinct and antagonistic CLE peptide pathways intersects to produce and specify different tissue layers in the
Arabidopsis
root tip. Their quantitative modulation is required to guide phloem initiation and differentiation. |
| doi_str_mv | 10.1038/s41477-024-01838-1 |
| format | Article |
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Arabidopsis
shoot meristems by signalling through redundant and cross-compensating CLAVATA1 (CLV1)-type receptor kinases. In the root meristem, the CLV1 homologues BARELY ANY MERISTEM 1 (BAM1) and BAM2 drive CLE13/16-mediated formative divisions that produce the ground tissue layers. Here we report that BAM1/2 are also required to initiate the vascular phloem lineage and that cross-compensation between CLV1-type receptors as observed in the shoot does not operate similarly in the root. Rather, we find that BAM3-mediated CLE45 signalling antagonizes BAM1/2-mediated CLE11/12/13 signalling in the phloem initials but not in the ground tissue. We further observe spatiotemporally contrasting CLE signalling requirements for phloem initiation and differentiation, which are shaped by the SHORT ROOT (SHR) pathway. Our findings thus suggest an intricate quantitative interplay between distinct and antagonistic CLE signalling pathways that organizes tissue layer formation in the
Arabidopsis
root meristem.
The activity of distinct and antagonistic CLE peptide pathways intersects to produce and specify different tissue layers in the
Arabidopsis
root tip. Their quantitative modulation is required to guide phloem initiation and differentiation.</description><identifier>ISSN: 2055-0278</identifier><identifier>EISSN: 2055-0278</identifier><identifier>DOI: 10.1038/s41477-024-01838-1</identifier><identifier>PMID: 39468296</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13/106 ; 14/19 ; 14/35 ; 38/39 ; 38/91 ; 631/449/2653/1974 ; 631/449/2653/2654 ; 631/449/2675 ; Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Biomedical and Life Sciences ; Differentiation ; Gene Expression Regulation, Plant ; Kinases ; Letter ; Life Sciences ; Membrane Proteins ; Meristem - genetics ; Meristem - growth & development ; Meristem - metabolism ; Meristems ; Pattern formation ; Peptides ; Phloem ; Phloem - growth & development ; Phloem - metabolism ; Plant Roots - growth & development ; Plant Roots - metabolism ; Plant Sciences ; Protein Serine-Threonine Kinases - genetics ; Protein Serine-Threonine Kinases - metabolism ; Receptors ; Signal Transduction ; Stem cells</subject><ispartof>Nature plants, 2024-12, Vol.10 (12), p.1900-1908</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><rights>2024. The Author(s), under exclusive licence to Springer Nature Limited.</rights><rights>Copyright Nature Publishing Group Dec 2024</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c256t-1480b643a4d858c5e8b349afa69db220d871c564887ec46ebf2e5b2c96c74f23</cites><orcidid>0000-0001-9065-8794 ; 0000-0003-3203-1058 ; 0000-0003-1113-1252</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/s41477-024-01838-1$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41477-024-01838-1$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27923,27924,41487,42556,51318</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39468296$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Hang</creatorcontrib><creatorcontrib>Wang, Qian</creatorcontrib><creatorcontrib>Blanco-Touriñán, Noel</creatorcontrib><creatorcontrib>Hardtke, Christian S.</creatorcontrib><title>Antagonistic CLE peptide pathways shape root meristem tissue patterning</title><title>Nature plants</title><addtitle>Nat. Plants</addtitle><addtitle>Nat Plants</addtitle><description>Secreted CLAVATA3/EMBRYO SURROUNDING REGION (CLE) peptide ligands dimension the stem cell niche of
Arabidopsis
shoot meristems by signalling through redundant and cross-compensating CLAVATA1 (CLV1)-type receptor kinases. In the root meristem, the CLV1 homologues BARELY ANY MERISTEM 1 (BAM1) and BAM2 drive CLE13/16-mediated formative divisions that produce the ground tissue layers. Here we report that BAM1/2 are also required to initiate the vascular phloem lineage and that cross-compensation between CLV1-type receptors as observed in the shoot does not operate similarly in the root. Rather, we find that BAM3-mediated CLE45 signalling antagonizes BAM1/2-mediated CLE11/12/13 signalling in the phloem initials but not in the ground tissue. We further observe spatiotemporally contrasting CLE signalling requirements for phloem initiation and differentiation, which are shaped by the SHORT ROOT (SHR) pathway. Our findings thus suggest an intricate quantitative interplay between distinct and antagonistic CLE signalling pathways that organizes tissue layer formation in the
Arabidopsis
root meristem.
The activity of distinct and antagonistic CLE peptide pathways intersects to produce and specify different tissue layers in the
Arabidopsis
root tip. Their quantitative modulation is required to guide phloem initiation and differentiation.</description><subject>13/106</subject><subject>14/19</subject><subject>14/35</subject><subject>38/39</subject><subject>38/91</subject><subject>631/449/2653/1974</subject><subject>631/449/2653/2654</subject><subject>631/449/2675</subject><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Biomedical and Life Sciences</subject><subject>Differentiation</subject><subject>Gene Expression Regulation, Plant</subject><subject>Kinases</subject><subject>Letter</subject><subject>Life Sciences</subject><subject>Membrane Proteins</subject><subject>Meristem - genetics</subject><subject>Meristem - growth & development</subject><subject>Meristem - metabolism</subject><subject>Meristems</subject><subject>Pattern formation</subject><subject>Peptides</subject><subject>Phloem</subject><subject>Phloem - growth & development</subject><subject>Phloem - metabolism</subject><subject>Plant Roots - growth & development</subject><subject>Plant Roots - metabolism</subject><subject>Plant Sciences</subject><subject>Protein Serine-Threonine Kinases - genetics</subject><subject>Protein Serine-Threonine Kinases - metabolism</subject><subject>Receptors</subject><subject>Signal Transduction</subject><subject>Stem cells</subject><issn>2055-0278</issn><issn>2055-0278</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kMtKAzEUhoMoKtoXcCEDbtyM5p7MshRvUHDTfchkzrRTOheTDNK3N7X1ggtXCcn3_-fwIXRF8B3BTN8HTrhSOaY8x0QznZMjdE6xEOlJ6eNf9zM0CWGNMSZKCCbxKTpjBZeaFvIcPU27aJd914TYuGw2f8gGGGJTQTbYuHq325CFlR0g830fsxZ8AqHNYhPC-MlE8F3TLS_RSW03ASaH8wItHh8Ws-d8_vr0MpvOc0eFjDnhGpeSM8srLbQToEvGC1tbWVQlpbjSijghudYKHJdQ1hRESV0hneI1ZRfodl87-P5thBBN2wQHm43toB-DYYQSUTBKd-jNH3Tdj75LyyWKC6qkkixRdE8534fgoTaDb1rrt4ZgsxNt9qJNEm0-RRuSQteH6rFsofqOfGlNANsDIX11S_A_s_-p_QCFiofA</recordid><startdate>20241201</startdate><enddate>20241201</enddate><creator>Zhang, Hang</creator><creator>Wang, Qian</creator><creator>Blanco-Touriñán, Noel</creator><creator>Hardtke, Christian S.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>7SN</scope><scope>C1K</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-9065-8794</orcidid><orcidid>https://orcid.org/0000-0003-3203-1058</orcidid><orcidid>https://orcid.org/0000-0003-1113-1252</orcidid></search><sort><creationdate>20241201</creationdate><title>Antagonistic CLE peptide pathways shape root meristem tissue patterning</title><author>Zhang, Hang ; Wang, Qian ; Blanco-Touriñán, Noel ; Hardtke, Christian S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c256t-1480b643a4d858c5e8b349afa69db220d871c564887ec46ebf2e5b2c96c74f23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>13/106</topic><topic>14/19</topic><topic>14/35</topic><topic>38/39</topic><topic>38/91</topic><topic>631/449/2653/1974</topic><topic>631/449/2653/2654</topic><topic>631/449/2675</topic><topic>Arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Biomedical and Life Sciences</topic><topic>Differentiation</topic><topic>Gene Expression Regulation, Plant</topic><topic>Kinases</topic><topic>Letter</topic><topic>Life Sciences</topic><topic>Membrane Proteins</topic><topic>Meristem - genetics</topic><topic>Meristem - growth & development</topic><topic>Meristem - metabolism</topic><topic>Meristems</topic><topic>Pattern formation</topic><topic>Peptides</topic><topic>Phloem</topic><topic>Phloem - growth & development</topic><topic>Phloem - metabolism</topic><topic>Plant Roots - growth & development</topic><topic>Plant Roots - metabolism</topic><topic>Plant Sciences</topic><topic>Protein Serine-Threonine Kinases - genetics</topic><topic>Protein Serine-Threonine Kinases - metabolism</topic><topic>Receptors</topic><topic>Signal Transduction</topic><topic>Stem cells</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Hang</creatorcontrib><creatorcontrib>Wang, Qian</creatorcontrib><creatorcontrib>Blanco-Touriñán, Noel</creatorcontrib><creatorcontrib>Hardtke, Christian S.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><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>Zhang, Hang</au><au>Wang, Qian</au><au>Blanco-Touriñán, Noel</au><au>Hardtke, Christian S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Antagonistic CLE peptide pathways shape root meristem tissue patterning</atitle><jtitle>Nature plants</jtitle><stitle>Nat. Plants</stitle><addtitle>Nat Plants</addtitle><date>2024-12-01</date><risdate>2024</risdate><volume>10</volume><issue>12</issue><spage>1900</spage><epage>1908</epage><pages>1900-1908</pages><issn>2055-0278</issn><eissn>2055-0278</eissn><abstract>Secreted CLAVATA3/EMBRYO SURROUNDING REGION (CLE) peptide ligands dimension the stem cell niche of
Arabidopsis
shoot meristems by signalling through redundant and cross-compensating CLAVATA1 (CLV1)-type receptor kinases. In the root meristem, the CLV1 homologues BARELY ANY MERISTEM 1 (BAM1) and BAM2 drive CLE13/16-mediated formative divisions that produce the ground tissue layers. Here we report that BAM1/2 are also required to initiate the vascular phloem lineage and that cross-compensation between CLV1-type receptors as observed in the shoot does not operate similarly in the root. Rather, we find that BAM3-mediated CLE45 signalling antagonizes BAM1/2-mediated CLE11/12/13 signalling in the phloem initials but not in the ground tissue. We further observe spatiotemporally contrasting CLE signalling requirements for phloem initiation and differentiation, which are shaped by the SHORT ROOT (SHR) pathway. Our findings thus suggest an intricate quantitative interplay between distinct and antagonistic CLE signalling pathways that organizes tissue layer formation in the
Arabidopsis
root meristem.
The activity of distinct and antagonistic CLE peptide pathways intersects to produce and specify different tissue layers in the
Arabidopsis
root tip. Their quantitative modulation is required to guide phloem initiation and differentiation.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>39468296</pmid><doi>10.1038/s41477-024-01838-1</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0001-9065-8794</orcidid><orcidid>https://orcid.org/0000-0003-3203-1058</orcidid><orcidid>https://orcid.org/0000-0003-1113-1252</orcidid></addata></record> |
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| subjects | 13/106 14/19 14/35 38/39 38/91 631/449/2653/1974 631/449/2653/2654 631/449/2675 Arabidopsis Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Biomedical and Life Sciences Differentiation Gene Expression Regulation, Plant Kinases Letter Life Sciences Membrane Proteins Meristem - genetics Meristem - growth & development Meristem - metabolism Meristems Pattern formation Peptides Phloem Phloem - growth & development Phloem - metabolism Plant Roots - growth & development Plant Roots - metabolism Plant Sciences Protein Serine-Threonine Kinases - genetics Protein Serine-Threonine Kinases - metabolism Receptors Signal Transduction Stem cells |
| title | Antagonistic CLE peptide pathways shape root meristem tissue patterning |
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