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Development of an evolutionarily novel structure: Fibroblast growth factor expression in the carapacial ridge of turtle embryos
The turtle shell, an evolutionarily novel structure, contains a bony exoskeleton that includes a dorsal carapace and a ventral plastron. The development of the carapace is dependent on the carapacial ridge (CR), a bulge in the dorsal flank that contains an ectodermal structure analogous to the apica...
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Published in: | The Journal of experimental zoology 2001-10, Vol.291 (3), p.274-281 |
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container_title | The Journal of experimental zoology |
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creator | Loredo, Grace A. Brukman, Alla Harris, Matthew P. Kagle, David Leclair, Elizabeth E. Gutman, Rachel Denney, Erin Henkelman, Emily Murray, B. Patrick Fallon, John F. Tuan, Rocky S. Gilbert, Scott F. |
description | The turtle shell, an evolutionarily novel structure, contains a bony exoskeleton that includes a dorsal carapace and a ventral plastron. The development of the carapace is dependent on the carapacial ridge (CR), a bulge in the dorsal flank that contains an ectodermal structure analogous to the apical ectodermal ridge (AER) of the developing limb (Burke. 1989a. J Morphol 199:363–378; Burke. 1989b. Fortschr Zool 35:206–209). Although the CR is thought to mediate the initiation and outgrowth of the carapace, the mechanisms of shell development have not been studied on the molecular level. Here, we present data suggesting that carapace formation is initiated by co‐opting genes that had other functions in the ancestral embryo, specifically those of limb outgrowth. However, there is divergence in the signaling repertoire from that involved in limb initiation and outgrowth. In situ hybridizations with antisense riboprobes derived from Trionyx spiniferous fibroblast growth factor‐10 (tfgf10) and Trachemys scripta (T. scripta) fibroblast‐growth factor 8 (tfgf8) cDNAs were performed on sections of early T. scripta embryos (< 30 days). Expression of tfgf10 was localized to the mesenchyme subjacent to the ectoderm of the CR. In the chick limb bud, FGF10 is known to be expressed in the early limb‐forming mesenchyme and is capable of inducing FGF8 in the AER to initiate the outgrowth of the limb bud. Although the expression of tfgf8 was found in the AER of the developing turtle limb, it was not seen in the CR. Thus, the initiation of the carapace is in agreement with FGF10 expression in the CR, but FGF8 does not appear to have a role in mediating early carapace outgrowth. J. Exp. Zool. (Mol. Dev. Evol.) 291:274–281, 2001. © 2001 Wiley‐Liss, Inc. |
doi_str_mv | 10.1002/jez.1103 |
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Patrick ; Fallon, John F. ; Tuan, Rocky S. ; Gilbert, Scott F.</creator><creatorcontrib>Loredo, Grace A. ; Brukman, Alla ; Harris, Matthew P. ; Kagle, David ; Leclair, Elizabeth E. ; Gutman, Rachel ; Denney, Erin ; Henkelman, Emily ; Murray, B. Patrick ; Fallon, John F. ; Tuan, Rocky S. ; Gilbert, Scott F.</creatorcontrib><description>The turtle shell, an evolutionarily novel structure, contains a bony exoskeleton that includes a dorsal carapace and a ventral plastron. The development of the carapace is dependent on the carapacial ridge (CR), a bulge in the dorsal flank that contains an ectodermal structure analogous to the apical ectodermal ridge (AER) of the developing limb (Burke. 1989a. J Morphol 199:363–378; Burke. 1989b. Fortschr Zool 35:206–209). Although the CR is thought to mediate the initiation and outgrowth of the carapace, the mechanisms of shell development have not been studied on the molecular level. Here, we present data suggesting that carapace formation is initiated by co‐opting genes that had other functions in the ancestral embryo, specifically those of limb outgrowth. However, there is divergence in the signaling repertoire from that involved in limb initiation and outgrowth. In situ hybridizations with antisense riboprobes derived from Trionyx spiniferous fibroblast growth factor‐10 (tfgf10) and Trachemys scripta (T. scripta) fibroblast‐growth factor 8 (tfgf8) cDNAs were performed on sections of early T. scripta embryos (< 30 days). Expression of tfgf10 was localized to the mesenchyme subjacent to the ectoderm of the CR. In the chick limb bud, FGF10 is known to be expressed in the early limb‐forming mesenchyme and is capable of inducing FGF8 in the AER to initiate the outgrowth of the limb bud. Although the expression of tfgf8 was found in the AER of the developing turtle limb, it was not seen in the CR. Thus, the initiation of the carapace is in agreement with FGF10 expression in the CR, but FGF8 does not appear to have a role in mediating early carapace outgrowth. J. Exp. Zool. (Mol. Dev. 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Patrick</creatorcontrib><creatorcontrib>Fallon, John F.</creatorcontrib><creatorcontrib>Tuan, Rocky S.</creatorcontrib><creatorcontrib>Gilbert, Scott F.</creatorcontrib><title>Development of an evolutionarily novel structure: Fibroblast growth factor expression in the carapacial ridge of turtle embryos</title><title>The Journal of experimental zoology</title><addtitle>J. Exp. Zool</addtitle><description>The turtle shell, an evolutionarily novel structure, contains a bony exoskeleton that includes a dorsal carapace and a ventral plastron. The development of the carapace is dependent on the carapacial ridge (CR), a bulge in the dorsal flank that contains an ectodermal structure analogous to the apical ectodermal ridge (AER) of the developing limb (Burke. 1989a. J Morphol 199:363–378; Burke. 1989b. Fortschr Zool 35:206–209). Although the CR is thought to mediate the initiation and outgrowth of the carapace, the mechanisms of shell development have not been studied on the molecular level. Here, we present data suggesting that carapace formation is initiated by co‐opting genes that had other functions in the ancestral embryo, specifically those of limb outgrowth. However, there is divergence in the signaling repertoire from that involved in limb initiation and outgrowth. In situ hybridizations with antisense riboprobes derived from Trionyx spiniferous fibroblast growth factor‐10 (tfgf10) and Trachemys scripta (T. scripta) fibroblast‐growth factor 8 (tfgf8) cDNAs were performed on sections of early T. scripta embryos (< 30 days). Expression of tfgf10 was localized to the mesenchyme subjacent to the ectoderm of the CR. In the chick limb bud, FGF10 is known to be expressed in the early limb‐forming mesenchyme and is capable of inducing FGF8 in the AER to initiate the outgrowth of the limb bud. Although the expression of tfgf8 was found in the AER of the developing turtle limb, it was not seen in the CR. Thus, the initiation of the carapace is in agreement with FGF10 expression in the CR, but FGF8 does not appear to have a role in mediating early carapace outgrowth. J. Exp. Zool. (Mol. Dev. Evol.) 291:274–281, 2001. © 2001 Wiley‐Liss, Inc.</description><subject>Animals</subject><subject>Base Sequence</subject><subject>Biological Evolution</subject><subject>Bone Development - genetics</subject><subject>Embryonic Development</subject><subject>Fibroblast Growth Factors - biosynthesis</subject><subject>Fibroblast Growth Factors - pharmacology</subject><subject>Gene Expression Regulation, Developmental</subject><subject>In Situ Hybridization</subject><subject>Molecular Sequence Data</subject><subject>Turtles - anatomy & histology</subject><subject>Turtles - genetics</subject><subject>Turtles - growth & development</subject><issn>0022-104X</issn><issn>1097-010X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2001</creationdate><recordtype>article</recordtype><recordid>eNp1kE1v1DAQhq0K1C4FiV-AfEJcUux4Hce9Vf1GVXtgJSouluNMWrdOHGyn7XLhr-PVRvTE6T3MM89oXoQ-UnJACSm_PsDvA0oJ20ELSqQoCCW3b9Aij8qCkuXtHnoX4wMhlHIidtFeTllLyhfozwk8gfNjD0PCvsN6wPDk3ZSsH3Swbo0HnwEcU5hMmgIc4jPbBN84HRO-C_453eNOm-QDhpcxQIx5E9sBp3vARgc9amO1w8G2d7C5kCXJAYa-CWsf36O3nXYRPsy5j1Znp6vji-Lq5vzy-OiqMMuSsqImDWtlyw3tuAS95KwknJumq4wAWGpedbqtylJKU_NKMF1D1dKmaoQGCYbto89b7Rj8rwliUr2NBpzTA_gpKlFSKWhZZ_DLFjTBxxigU2OwvQ5rRYnadK1y12rTdUY_zc6p6aF9BedyM1BsgWfrYP1fkfp2-nMWzryNCV7-8To8qvyS4OrH9bla1ZU4-c6YqthfNd6axw</recordid><startdate>20011015</startdate><enddate>20011015</enddate><creator>Loredo, Grace A.</creator><creator>Brukman, Alla</creator><creator>Harris, Matthew P.</creator><creator>Kagle, David</creator><creator>Leclair, Elizabeth E.</creator><creator>Gutman, Rachel</creator><creator>Denney, Erin</creator><creator>Henkelman, Emily</creator><creator>Murray, B. 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Patrick</creatorcontrib><creatorcontrib>Fallon, John F.</creatorcontrib><creatorcontrib>Tuan, Rocky S.</creatorcontrib><creatorcontrib>Gilbert, Scott F.</creatorcontrib><collection>Istex</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>The Journal of experimental zoology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Loredo, Grace A.</au><au>Brukman, Alla</au><au>Harris, Matthew P.</au><au>Kagle, David</au><au>Leclair, Elizabeth E.</au><au>Gutman, Rachel</au><au>Denney, Erin</au><au>Henkelman, Emily</au><au>Murray, B. Patrick</au><au>Fallon, John F.</au><au>Tuan, Rocky S.</au><au>Gilbert, Scott F.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Development of an evolutionarily novel structure: Fibroblast growth factor expression in the carapacial ridge of turtle embryos</atitle><jtitle>The Journal of experimental zoology</jtitle><addtitle>J. Exp. Zool</addtitle><date>2001-10-15</date><risdate>2001</risdate><volume>291</volume><issue>3</issue><spage>274</spage><epage>281</epage><pages>274-281</pages><issn>0022-104X</issn><eissn>1097-010X</eissn><abstract>The turtle shell, an evolutionarily novel structure, contains a bony exoskeleton that includes a dorsal carapace and a ventral plastron. The development of the carapace is dependent on the carapacial ridge (CR), a bulge in the dorsal flank that contains an ectodermal structure analogous to the apical ectodermal ridge (AER) of the developing limb (Burke. 1989a. J Morphol 199:363–378; Burke. 1989b. Fortschr Zool 35:206–209). Although the CR is thought to mediate the initiation and outgrowth of the carapace, the mechanisms of shell development have not been studied on the molecular level. Here, we present data suggesting that carapace formation is initiated by co‐opting genes that had other functions in the ancestral embryo, specifically those of limb outgrowth. However, there is divergence in the signaling repertoire from that involved in limb initiation and outgrowth. In situ hybridizations with antisense riboprobes derived from Trionyx spiniferous fibroblast growth factor‐10 (tfgf10) and Trachemys scripta (T. scripta) fibroblast‐growth factor 8 (tfgf8) cDNAs were performed on sections of early T. scripta embryos (< 30 days). Expression of tfgf10 was localized to the mesenchyme subjacent to the ectoderm of the CR. In the chick limb bud, FGF10 is known to be expressed in the early limb‐forming mesenchyme and is capable of inducing FGF8 in the AER to initiate the outgrowth of the limb bud. Although the expression of tfgf8 was found in the AER of the developing turtle limb, it was not seen in the CR. Thus, the initiation of the carapace is in agreement with FGF10 expression in the CR, but FGF8 does not appear to have a role in mediating early carapace outgrowth. J. Exp. Zool. (Mol. Dev. Evol.) 291:274–281, 2001. © 2001 Wiley‐Liss, Inc.</abstract><cop>New York</cop><pub>John Wiley & Sons, Inc</pub><pmid>11598915</pmid><doi>10.1002/jez.1103</doi><tpages>8</tpages></addata></record> |
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subjects | Animals Base Sequence Biological Evolution Bone Development - genetics Embryonic Development Fibroblast Growth Factors - biosynthesis Fibroblast Growth Factors - pharmacology Gene Expression Regulation, Developmental In Situ Hybridization Molecular Sequence Data Turtles - anatomy & histology Turtles - genetics Turtles - growth & development |
title | Development of an evolutionarily novel structure: Fibroblast growth factor expression in the carapacial ridge of turtle embryos |
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