Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta
It has been posited that animal development evolved from pre-existing mechanisms for regulating cell differentiation in the single celled and colonial ancestors of animals. Although the progenitors of animals cannot be studied directly, insights into their cell biology may be gleaned from comparison...
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Veröffentlicht in: | Developmental biology 2011-09, Vol.357 (1), p.73-82 |
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creator | Dayel, Mark J. Alegado, Rosanna A. Fairclough, Stephen R. Levin, Tera C. Nichols, Scott A. McDonald, Kent King, Nicole |
description | It has been posited that animal development evolved from pre-existing mechanisms for regulating cell differentiation in the single celled and colonial ancestors of animals. Although the progenitors of animals cannot be studied directly, insights into their cell biology may be gleaned from comparisons between animals and their closest living relatives, the choanoflagellates. We report here on the life history, cell differentiation and intercellular interactions in the colony-forming choanoflagellate Salpingoeca rosetta. In response to diverse environmental cues, S. rosetta differentiates into at least five distinct cell types, including three solitary cell types (slow swimmers, fast swimmers, and thecate cells) and two colonial forms (rosettes and chains). Electron microscopy reveals that cells within colonies are held together by a combination of fine intercellular bridges, a shared extracellular matrix, and filopodia. In addition, we have discovered that the carbohydrate-binding protein wheat germ agglutinin specifically stains colonies and the slow swimmers from which they form, showing that molecular differentiation precedes multicellular development. Together, these results help establish S. rosetta as a model system for studying simple multicellularity in choanoflagellates and provide an experimental framework for investigating the origin of animal multicellularity and development.
► Salpingoeca rosetta differentiates into at least five different single cell and colonial forms. ► WGA staining signals competence of single cells to develop into colonies. ► Cells in S. rosetta colonies interact through intercellular bridges, filopodia, and ECM. |
doi_str_mv | 10.1016/j.ydbio.2011.06.003 |
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► Salpingoeca rosetta differentiates into at least five different single cell and colonial forms. ► WGA staining signals competence of single cells to develop into colonies. ► Cells in S. rosetta colonies interact through intercellular bridges, filopodia, and ECM.</description><identifier>ISSN: 0012-1606</identifier><identifier>EISSN: 1095-564X</identifier><identifier>DOI: 10.1016/j.ydbio.2011.06.003</identifier><identifier>PMID: 21699890</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>agglutinins ; ancestry ; animal development ; Animals ; carbohydrate binding ; Cell Differentiation ; Choanoflagellata - cytology ; Choanoflagellata - metabolism ; Choanoflagellata - ultrastructure ; Choanoflagellate ; Colony ; Development ; electron microscopy ; extracellular matrix ; Intercellular bridges ; life history ; Microscopy, Electron, Scanning ; Morphogenesis ; Origin of animal multicellularity ; Proterospongia ; pseudopodia ; Receptors, Cell Surface - metabolism ; Salpingoeca ; Salpingoeca rosetta ; wheat germ ; wheat protein</subject><ispartof>Developmental biology, 2011-09, Vol.357 (1), p.73-82</ispartof><rights>2011 Elsevier Inc.</rights><rights>Copyright © 2011 Elsevier Inc. All rights reserved.</rights><rights>2011 Elsevier Inc. All rights reserved. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c590t-cfb51fc491ddb00931efac34a0b4481f1dfb90177e08f898e2b9f3868a22bc9a3</citedby><cites>FETCH-LOGICAL-c590t-cfb51fc491ddb00931efac34a0b4481f1dfb90177e08f898e2b9f3868a22bc9a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0012160611009924$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21699890$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Dayel, Mark J.</creatorcontrib><creatorcontrib>Alegado, Rosanna A.</creatorcontrib><creatorcontrib>Fairclough, Stephen R.</creatorcontrib><creatorcontrib>Levin, Tera C.</creatorcontrib><creatorcontrib>Nichols, Scott A.</creatorcontrib><creatorcontrib>McDonald, Kent</creatorcontrib><creatorcontrib>King, Nicole</creatorcontrib><title>Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta</title><title>Developmental biology</title><addtitle>Dev Biol</addtitle><description>It has been posited that animal development evolved from pre-existing mechanisms for regulating cell differentiation in the single celled and colonial ancestors of animals. Although the progenitors of animals cannot be studied directly, insights into their cell biology may be gleaned from comparisons between animals and their closest living relatives, the choanoflagellates. We report here on the life history, cell differentiation and intercellular interactions in the colony-forming choanoflagellate Salpingoeca rosetta. In response to diverse environmental cues, S. rosetta differentiates into at least five distinct cell types, including three solitary cell types (slow swimmers, fast swimmers, and thecate cells) and two colonial forms (rosettes and chains). Electron microscopy reveals that cells within colonies are held together by a combination of fine intercellular bridges, a shared extracellular matrix, and filopodia. In addition, we have discovered that the carbohydrate-binding protein wheat germ agglutinin specifically stains colonies and the slow swimmers from which they form, showing that molecular differentiation precedes multicellular development. Together, these results help establish S. rosetta as a model system for studying simple multicellularity in choanoflagellates and provide an experimental framework for investigating the origin of animal multicellularity and development.
► Salpingoeca rosetta differentiates into at least five different single cell and colonial forms. ► WGA staining signals competence of single cells to develop into colonies. ► Cells in S. rosetta colonies interact through intercellular bridges, filopodia, and ECM.</description><subject>agglutinins</subject><subject>ancestry</subject><subject>animal development</subject><subject>Animals</subject><subject>carbohydrate binding</subject><subject>Cell Differentiation</subject><subject>Choanoflagellata - cytology</subject><subject>Choanoflagellata - metabolism</subject><subject>Choanoflagellata - ultrastructure</subject><subject>Choanoflagellate</subject><subject>Colony</subject><subject>Development</subject><subject>electron microscopy</subject><subject>extracellular matrix</subject><subject>Intercellular bridges</subject><subject>life history</subject><subject>Microscopy, Electron, Scanning</subject><subject>Morphogenesis</subject><subject>Origin of animal multicellularity</subject><subject>Proterospongia</subject><subject>pseudopodia</subject><subject>Receptors, Cell Surface - metabolism</subject><subject>Salpingoeca</subject><subject>Salpingoeca rosetta</subject><subject>wheat germ</subject><subject>wheat protein</subject><issn>0012-1606</issn><issn>1095-564X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUFvEzEQhS0EomnhFyChvcFll_Ha69gHkFDUQqVKHACJm-X1jhNHu3awN5Xy73GaUsGl6smH-eaN33uEvKHQUKDiw7Y5DL2PTQuUNiAaAPaMLCioru4E__WcLABoW1MB4oyc57yFQkjJXpKzlgqlpIIFMSscx2rwzmHCMHsz-xgqE4Zqimm3iWsMmH2ufKjmDVY2jjEcahfT5MO6sptoQnSjWRcVM2P13Yy7MohoTZVixnk2r8gLZ8aMr-_fC_Lz6vLH6mt98-3L9erzTW07BXNtXd9RZ7miw9ADKEbRGcu4gZ5zSR0dXK-ALpcI0kklse2VY1JI07a9VYZdkE8n3d2-n3CwxU0yo94lP5l00NF4_f8k-I1ex1vNaCeYaovAu3uBFH_vMc968tkejQWM-6xLdJIveccL-f5RkkpgFCSHJ6Adh5appYCCshNqS3I5oXv4OwV9bFxv9V3j-ti4BqFLn2Xr7b-2H3b-VlyAjycAS_i3HpPO1mOwOPiEdtZD9I8e-AMrhMCU</recordid><startdate>20110901</startdate><enddate>20110901</enddate><creator>Dayel, Mark J.</creator><creator>Alegado, Rosanna A.</creator><creator>Fairclough, Stephen R.</creator><creator>Levin, Tera C.</creator><creator>Nichols, Scott A.</creator><creator>McDonald, Kent</creator><creator>King, Nicole</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>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>7S9</scope><scope>L.6</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20110901</creationdate><title>Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta</title><author>Dayel, Mark J. ; Alegado, Rosanna A. ; Fairclough, Stephen R. ; Levin, Tera C. ; Nichols, Scott A. ; McDonald, Kent ; King, Nicole</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c590t-cfb51fc491ddb00931efac34a0b4481f1dfb90177e08f898e2b9f3868a22bc9a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>agglutinins</topic><topic>ancestry</topic><topic>animal development</topic><topic>Animals</topic><topic>carbohydrate binding</topic><topic>Cell Differentiation</topic><topic>Choanoflagellata - cytology</topic><topic>Choanoflagellata - metabolism</topic><topic>Choanoflagellata - ultrastructure</topic><topic>Choanoflagellate</topic><topic>Colony</topic><topic>Development</topic><topic>electron microscopy</topic><topic>extracellular matrix</topic><topic>Intercellular bridges</topic><topic>life history</topic><topic>Microscopy, Electron, Scanning</topic><topic>Morphogenesis</topic><topic>Origin of animal multicellularity</topic><topic>Proterospongia</topic><topic>pseudopodia</topic><topic>Receptors, Cell Surface - metabolism</topic><topic>Salpingoeca</topic><topic>Salpingoeca rosetta</topic><topic>wheat germ</topic><topic>wheat protein</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dayel, Mark J.</creatorcontrib><creatorcontrib>Alegado, Rosanna A.</creatorcontrib><creatorcontrib>Fairclough, Stephen R.</creatorcontrib><creatorcontrib>Levin, Tera C.</creatorcontrib><creatorcontrib>Nichols, Scott A.</creatorcontrib><creatorcontrib>McDonald, Kent</creatorcontrib><creatorcontrib>King, Nicole</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>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Developmental biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dayel, Mark J.</au><au>Alegado, Rosanna A.</au><au>Fairclough, Stephen R.</au><au>Levin, Tera C.</au><au>Nichols, Scott A.</au><au>McDonald, Kent</au><au>King, Nicole</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta</atitle><jtitle>Developmental biology</jtitle><addtitle>Dev Biol</addtitle><date>2011-09-01</date><risdate>2011</risdate><volume>357</volume><issue>1</issue><spage>73</spage><epage>82</epage><pages>73-82</pages><issn>0012-1606</issn><eissn>1095-564X</eissn><abstract>It has been posited that animal development evolved from pre-existing mechanisms for regulating cell differentiation in the single celled and colonial ancestors of animals. Although the progenitors of animals cannot be studied directly, insights into their cell biology may be gleaned from comparisons between animals and their closest living relatives, the choanoflagellates. We report here on the life history, cell differentiation and intercellular interactions in the colony-forming choanoflagellate Salpingoeca rosetta. In response to diverse environmental cues, S. rosetta differentiates into at least five distinct cell types, including three solitary cell types (slow swimmers, fast swimmers, and thecate cells) and two colonial forms (rosettes and chains). Electron microscopy reveals that cells within colonies are held together by a combination of fine intercellular bridges, a shared extracellular matrix, and filopodia. In addition, we have discovered that the carbohydrate-binding protein wheat germ agglutinin specifically stains colonies and the slow swimmers from which they form, showing that molecular differentiation precedes multicellular development. Together, these results help establish S. rosetta as a model system for studying simple multicellularity in choanoflagellates and provide an experimental framework for investigating the origin of animal multicellularity and development.
► Salpingoeca rosetta differentiates into at least five different single cell and colonial forms. ► WGA staining signals competence of single cells to develop into colonies. ► Cells in S. rosetta colonies interact through intercellular bridges, filopodia, and ECM.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>21699890</pmid><doi>10.1016/j.ydbio.2011.06.003</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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subjects | agglutinins ancestry animal development Animals carbohydrate binding Cell Differentiation Choanoflagellata - cytology Choanoflagellata - metabolism Choanoflagellata - ultrastructure Choanoflagellate Colony Development electron microscopy extracellular matrix Intercellular bridges life history Microscopy, Electron, Scanning Morphogenesis Origin of animal multicellularity Proterospongia pseudopodia Receptors, Cell Surface - metabolism Salpingoeca Salpingoeca rosetta wheat germ wheat protein |
title | Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta |
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