Moderation of Arabidopsis Root Stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 Receptor Kinase Complexes
The root system of higher plants originates from the activity of a root meristem, which comprises a group of highly specialized and long-lasting stem cells. Their maintenance and number is controlled by the quiescent center (QC) cells and by feedback signaling from differentiated cells. Root meriste...
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| Veröffentlicht in: | Current biology 2013-03, Vol.23 (5), p.362-371 |
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| creator | Stahl, Yvonne Grabowski, Stephanie Bleckmann, Andrea Kühnemuth, Ralf Weidtkamp-Peters, Stefanie Pinto, Karine Gustavo Kirschner, Gwendolyn K. Schmid, Julia B. Wink, René H. Hülsewede, Adrian Felekyan, Suren Seidel, Claus A.M. Simon, Rüdiger |
| description | The root system of higher plants originates from the activity of a root meristem, which comprises a group of highly specialized and long-lasting stem cells. Their maintenance and number is controlled by the quiescent center (QC) cells and by feedback signaling from differentiated cells. Root meristems may have evolved from structurally distinct shoot meristems; however, no common player acting in stemness control has been found so far.
We show that CLAVATA1 (CLV1), a key receptor kinase in shoot stemness maintenance, performs a similar but distinct role in root meristems. We report that CLV1 is signaling, activated by the peptide ligand CLAVATA3/EMBRYO SURROUNDING REGION40 (CLE40), together with the receptor kinase ARABIDOPSIS CRINKLY4 (ACR4) to restrict root stemness. Both CLV1 and ACR4 overlap in their expression domains in the distal root meristem and localize to the plasma membrane (PM) and plasmodesmata (PDs), where ACR4 preferentially accumulates. Using multiparameter fluorescence image spectroscopy (MFIS), we show that CLV1 and ACR4 can form homo- and heteromeric complexes that differ in their composition depending on their subcellular localization.
We hypothesize that these homo- and heteromeric complexes may differentially regulate distal root meristem maintenance. We conclude that essential components of the ancestral shoot stemness regulatory system also act in the root and that the specific interaction of CLV1 with ACR4 serves to moderate and control stemness homeostasis in the root meristem. The structural differences between these two meristem types may have necessitated this recruitment of ACR4 for signaling by CLV1.
[Display omitted]
► CLV1 receptor kinase regulates stemness in Arabidopsis root and shoot meristems ► CLV1 and ACR4 form homo- and heteromeric complexes as shown by a novel FRET assay ► CLV1/ACR4 complexes differ in composition between plasma membrane and plasmodesmata ► CLV1/ACR4 complexes regulate distal root meristem maintenance |
| doi_str_mv | 10.1016/j.cub.2013.01.045 |
| format | Article |
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We show that CLAVATA1 (CLV1), a key receptor kinase in shoot stemness maintenance, performs a similar but distinct role in root meristems. We report that CLV1 is signaling, activated by the peptide ligand CLAVATA3/EMBRYO SURROUNDING REGION40 (CLE40), together with the receptor kinase ARABIDOPSIS CRINKLY4 (ACR4) to restrict root stemness. Both CLV1 and ACR4 overlap in their expression domains in the distal root meristem and localize to the plasma membrane (PM) and plasmodesmata (PDs), where ACR4 preferentially accumulates. Using multiparameter fluorescence image spectroscopy (MFIS), we show that CLV1 and ACR4 can form homo- and heteromeric complexes that differ in their composition depending on their subcellular localization.
We hypothesize that these homo- and heteromeric complexes may differentially regulate distal root meristem maintenance. We conclude that essential components of the ancestral shoot stemness regulatory system also act in the root and that the specific interaction of CLV1 with ACR4 serves to moderate and control stemness homeostasis in the root meristem. The structural differences between these two meristem types may have necessitated this recruitment of ACR4 for signaling by CLV1.
[Display omitted]
► CLV1 receptor kinase regulates stemness in Arabidopsis root and shoot meristems ► CLV1 and ACR4 form homo- and heteromeric complexes as shown by a novel FRET assay ► CLV1/ACR4 complexes differ in composition between plasma membrane and plasmodesmata ► CLV1/ACR4 complexes regulate distal root meristem maintenance</description><identifier>ISSN: 0960-9822</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2013.01.045</identifier><identifier>PMID: 23394827</identifier><language>eng</language><publisher>England: Elsevier Inc</publisher><subject>Arabidopsis ; Arabidopsis - enzymology ; Arabidopsis - growth & development ; Arabidopsis Proteins - metabolism ; fluorescence ; Fluorescence Resonance Energy Transfer ; homeostasis ; Meristem - enzymology ; Meristem - growth & development ; Plant Roots - enzymology ; Plant Roots - growth & development ; plasma membrane ; plasmodesmata ; Plasmodesmata - metabolism ; Protein-Serine-Threonine Kinases - metabolism ; Receptor Protein-Tyrosine Kinases - metabolism ; Receptors, Cell Surface - metabolism ; root meristems ; root systems ; shoot meristems ; spectroscopy ; stem cells</subject><ispartof>Current biology, 2013-03, Vol.23 (5), p.362-371</ispartof><rights>2013 Elsevier Ltd</rights><rights>Copyright © 2013 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4015-6ceb65909abac3504dc5f3eae5698291341dd49d8f089e99ad9822262fca5e7f3</citedby><cites>FETCH-LOGICAL-c4015-6ceb65909abac3504dc5f3eae5698291341dd49d8f089e99ad9822262fca5e7f3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0960982213000808$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23394827$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Stahl, Yvonne</creatorcontrib><creatorcontrib>Grabowski, Stephanie</creatorcontrib><creatorcontrib>Bleckmann, Andrea</creatorcontrib><creatorcontrib>Kühnemuth, Ralf</creatorcontrib><creatorcontrib>Weidtkamp-Peters, Stefanie</creatorcontrib><creatorcontrib>Pinto, Karine Gustavo</creatorcontrib><creatorcontrib>Kirschner, Gwendolyn K.</creatorcontrib><creatorcontrib>Schmid, Julia B.</creatorcontrib><creatorcontrib>Wink, René H.</creatorcontrib><creatorcontrib>Hülsewede, Adrian</creatorcontrib><creatorcontrib>Felekyan, Suren</creatorcontrib><creatorcontrib>Seidel, Claus A.M.</creatorcontrib><creatorcontrib>Simon, Rüdiger</creatorcontrib><title>Moderation of Arabidopsis Root Stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 Receptor Kinase Complexes</title><title>Current biology</title><addtitle>Curr Biol</addtitle><description>The root system of higher plants originates from the activity of a root meristem, which comprises a group of highly specialized and long-lasting stem cells. Their maintenance and number is controlled by the quiescent center (QC) cells and by feedback signaling from differentiated cells. Root meristems may have evolved from structurally distinct shoot meristems; however, no common player acting in stemness control has been found so far.
We show that CLAVATA1 (CLV1), a key receptor kinase in shoot stemness maintenance, performs a similar but distinct role in root meristems. We report that CLV1 is signaling, activated by the peptide ligand CLAVATA3/EMBRYO SURROUNDING REGION40 (CLE40), together with the receptor kinase ARABIDOPSIS CRINKLY4 (ACR4) to restrict root stemness. Both CLV1 and ACR4 overlap in their expression domains in the distal root meristem and localize to the plasma membrane (PM) and plasmodesmata (PDs), where ACR4 preferentially accumulates. Using multiparameter fluorescence image spectroscopy (MFIS), we show that CLV1 and ACR4 can form homo- and heteromeric complexes that differ in their composition depending on their subcellular localization.
We hypothesize that these homo- and heteromeric complexes may differentially regulate distal root meristem maintenance. We conclude that essential components of the ancestral shoot stemness regulatory system also act in the root and that the specific interaction of CLV1 with ACR4 serves to moderate and control stemness homeostasis in the root meristem. The structural differences between these two meristem types may have necessitated this recruitment of ACR4 for signaling by CLV1.
[Display omitted]
► CLV1 receptor kinase regulates stemness in Arabidopsis root and shoot meristems ► CLV1 and ACR4 form homo- and heteromeric complexes as shown by a novel FRET assay ► CLV1/ACR4 complexes differ in composition between plasma membrane and plasmodesmata ► CLV1/ACR4 complexes regulate distal root meristem maintenance</description><subject>Arabidopsis</subject><subject>Arabidopsis - enzymology</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>fluorescence</subject><subject>Fluorescence Resonance Energy Transfer</subject><subject>homeostasis</subject><subject>Meristem - enzymology</subject><subject>Meristem - growth & development</subject><subject>Plant Roots - enzymology</subject><subject>Plant Roots - growth & development</subject><subject>plasma membrane</subject><subject>plasmodesmata</subject><subject>Plasmodesmata - metabolism</subject><subject>Protein-Serine-Threonine Kinases - metabolism</subject><subject>Receptor Protein-Tyrosine Kinases - metabolism</subject><subject>Receptors, Cell Surface - metabolism</subject><subject>root meristems</subject><subject>root systems</subject><subject>shoot meristems</subject><subject>spectroscopy</subject><subject>stem cells</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kE1v1DAURS0EokPhB7ABL9kkfXbsTCxWIXx01IGimRaJleXYL8ijSRzsDKL_noymdNnV25x79e4h5DWDnAErL3a5PbQ5B1bkwHIQ8glZsGqpMhBCPiULUCVkquL8jLxIaQfAeKXK5-SMF4USFV8uSPc1OIxm8mGgoaN1NK13YUw-0U0IE91O2A-YEm3vaLOuf9Q3NaNmcLTe1B9WH6-_b1db2mxW367WPwXdoMVxCpFe-cEkpE3oxz3-xfSSPOvMPuGr-3tObj9_umkus_X1l1VTrzMrgMmstNiWUoEyrbGFBOGs7Ao0KMt5hmKFYM4J5aoOKoVKGXdcx0veWSNx2RXn5N2pd4zh9wHTpHufLO73ZsBwSJoVrAQpBFMzyk6ojSGliJ0eo-9NvNMM9FGv3ulZrz7q1cD0rHfOvLmvP7Q9uofEf58z8PYEdCZo8yv6pG-3c4MEgEJxCTPx_kTgrOGPx6iT9ThYdD6inbQL_pEH_gFaJJFh</recordid><startdate>20130304</startdate><enddate>20130304</enddate><creator>Stahl, Yvonne</creator><creator>Grabowski, Stephanie</creator><creator>Bleckmann, Andrea</creator><creator>Kühnemuth, Ralf</creator><creator>Weidtkamp-Peters, Stefanie</creator><creator>Pinto, Karine Gustavo</creator><creator>Kirschner, Gwendolyn K.</creator><creator>Schmid, Julia B.</creator><creator>Wink, René H.</creator><creator>Hülsewede, Adrian</creator><creator>Felekyan, Suren</creator><creator>Seidel, Claus A.M.</creator><creator>Simon, Rüdiger</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>FBQ</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></search><sort><creationdate>20130304</creationdate><title>Moderation of Arabidopsis Root Stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 Receptor Kinase Complexes</title><author>Stahl, Yvonne ; Grabowski, Stephanie ; Bleckmann, Andrea ; Kühnemuth, Ralf ; Weidtkamp-Peters, Stefanie ; Pinto, Karine Gustavo ; Kirschner, Gwendolyn K. ; Schmid, Julia B. ; Wink, René H. ; Hülsewede, Adrian ; Felekyan, Suren ; Seidel, Claus A.M. ; Simon, Rüdiger</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4015-6ceb65909abac3504dc5f3eae5698291341dd49d8f089e99ad9822262fca5e7f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - enzymology</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>fluorescence</topic><topic>Fluorescence Resonance Energy Transfer</topic><topic>homeostasis</topic><topic>Meristem - enzymology</topic><topic>Meristem - growth & development</topic><topic>Plant Roots - enzymology</topic><topic>Plant Roots - growth & development</topic><topic>plasma membrane</topic><topic>plasmodesmata</topic><topic>Plasmodesmata - metabolism</topic><topic>Protein-Serine-Threonine Kinases - metabolism</topic><topic>Receptor Protein-Tyrosine Kinases - metabolism</topic><topic>Receptors, Cell Surface - metabolism</topic><topic>root meristems</topic><topic>root systems</topic><topic>shoot meristems</topic><topic>spectroscopy</topic><topic>stem cells</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Stahl, Yvonne</creatorcontrib><creatorcontrib>Grabowski, Stephanie</creatorcontrib><creatorcontrib>Bleckmann, Andrea</creatorcontrib><creatorcontrib>Kühnemuth, Ralf</creatorcontrib><creatorcontrib>Weidtkamp-Peters, Stefanie</creatorcontrib><creatorcontrib>Pinto, Karine Gustavo</creatorcontrib><creatorcontrib>Kirschner, Gwendolyn K.</creatorcontrib><creatorcontrib>Schmid, Julia B.</creatorcontrib><creatorcontrib>Wink, René H.</creatorcontrib><creatorcontrib>Hülsewede, Adrian</creatorcontrib><creatorcontrib>Felekyan, Suren</creatorcontrib><creatorcontrib>Seidel, Claus A.M.</creatorcontrib><creatorcontrib>Simon, Rüdiger</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>AGRIS</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><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Stahl, Yvonne</au><au>Grabowski, Stephanie</au><au>Bleckmann, Andrea</au><au>Kühnemuth, Ralf</au><au>Weidtkamp-Peters, Stefanie</au><au>Pinto, Karine Gustavo</au><au>Kirschner, Gwendolyn K.</au><au>Schmid, Julia B.</au><au>Wink, René H.</au><au>Hülsewede, Adrian</au><au>Felekyan, Suren</au><au>Seidel, Claus A.M.</au><au>Simon, Rüdiger</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Moderation of Arabidopsis Root Stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 Receptor Kinase Complexes</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2013-03-04</date><risdate>2013</risdate><volume>23</volume><issue>5</issue><spage>362</spage><epage>371</epage><pages>362-371</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><abstract>The root system of higher plants originates from the activity of a root meristem, which comprises a group of highly specialized and long-lasting stem cells. Their maintenance and number is controlled by the quiescent center (QC) cells and by feedback signaling from differentiated cells. Root meristems may have evolved from structurally distinct shoot meristems; however, no common player acting in stemness control has been found so far.
We show that CLAVATA1 (CLV1), a key receptor kinase in shoot stemness maintenance, performs a similar but distinct role in root meristems. We report that CLV1 is signaling, activated by the peptide ligand CLAVATA3/EMBRYO SURROUNDING REGION40 (CLE40), together with the receptor kinase ARABIDOPSIS CRINKLY4 (ACR4) to restrict root stemness. Both CLV1 and ACR4 overlap in their expression domains in the distal root meristem and localize to the plasma membrane (PM) and plasmodesmata (PDs), where ACR4 preferentially accumulates. Using multiparameter fluorescence image spectroscopy (MFIS), we show that CLV1 and ACR4 can form homo- and heteromeric complexes that differ in their composition depending on their subcellular localization.
We hypothesize that these homo- and heteromeric complexes may differentially regulate distal root meristem maintenance. We conclude that essential components of the ancestral shoot stemness regulatory system also act in the root and that the specific interaction of CLV1 with ACR4 serves to moderate and control stemness homeostasis in the root meristem. The structural differences between these two meristem types may have necessitated this recruitment of ACR4 for signaling by CLV1.
[Display omitted]
► CLV1 receptor kinase regulates stemness in Arabidopsis root and shoot meristems ► CLV1 and ACR4 form homo- and heteromeric complexes as shown by a novel FRET assay ► CLV1/ACR4 complexes differ in composition between plasma membrane and plasmodesmata ► CLV1/ACR4 complexes regulate distal root meristem maintenance</abstract><cop>England</cop><pub>Elsevier Inc</pub><pmid>23394827</pmid><doi>10.1016/j.cub.2013.01.045</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Current biology, 2013-03, Vol.23 (5), p.362-371 |
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| source | MEDLINE; Cell Press Free Archives; Elsevier ScienceDirect Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
| subjects | Arabidopsis Arabidopsis - enzymology Arabidopsis - growth & development Arabidopsis Proteins - metabolism fluorescence Fluorescence Resonance Energy Transfer homeostasis Meristem - enzymology Meristem - growth & development Plant Roots - enzymology Plant Roots - growth & development plasma membrane plasmodesmata Plasmodesmata - metabolism Protein-Serine-Threonine Kinases - metabolism Receptor Protein-Tyrosine Kinases - metabolism Receptors, Cell Surface - metabolism root meristems root systems shoot meristems spectroscopy stem cells |
| title | Moderation of Arabidopsis Root Stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 Receptor Kinase Complexes |
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