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
Hauptverfasser: Dayel, Mark J., Alegado, Rosanna A., Fairclough, Stephen R., Levin, Tera C., Nichols, Scott A., McDonald, Kent, King, Nicole
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container_issue 1
container_start_page 73
container_title Developmental biology
container_volume 357
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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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><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. 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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. ; 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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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