Fin-fold development in paddlefish and catshark and implications for the evolution of the autopod.
Identifieur interne : 000C28 ( PubMed/Checkpoint ); précédent : 000C27; suivant : 000C29Fin-fold development in paddlefish and catshark and implications for the evolution of the autopod.
Auteurs : Frank J. Tulenko [États-Unis] ; James L. Massey [États-Unis] ; Elishka Holmquist [États-Unis] ; Gabriel Kigundu [États-Unis] ; Sarah Thomas [États-Unis] ; Susan M E. Smith [États-Unis] ; Sylvie Mazan [France] ; Marcus C. Davis [États-Unis]Source :
- Proceedings. Biological sciences [ 1471-2954 ] ; 2017.
Abstract
The evolutionary origin of the autopod involved a loss of the fin-fold and associated dermal skeleton with a concomitant elaboration of the distal endoskeleton to form a wrist and digits. Developmental studies, primarily from teleosts and amniotes, suggest a model for appendage evolution in which a delay in the AER-to-fin-fold conversion fuelled endoskeletal expansion by prolonging the function of AER-mediated regulatory networks. Here, we characterize aspects of paired fin development in the paddlefish Polyodon spathula (a non-teleost actinopterygian) and catshark Scyliorhinus canicula (chondrichthyan) to explore aspects of this model in a broader phylogenetic context. Our data demonstrate that in basal gnathostomes, the autopod marker HoxA13 co-localizes with the dermoskeleton component And1 to mark the position of the fin-fold, supporting recent work demonstrating a role for HoxA13 in zebrafish fin ray development. Additionally, we show that in paddlefish, the proximal fin and fin-fold mesenchyme share a common mesodermal origin, and that components of the Shh/LIM/Gremlin/Fgf transcriptional network critical to limb bud outgrowth and patterning are expressed in the fin-fold with a profile similar to that of tetrapods. Together these data draw contrast with hypotheses of AER heterochrony and suggest that limb-specific morphologies arose through evolutionary changes in the differentiation outcome of conserved early distal patterning compartments.
DOI: 10.1098/rspb.2016.2780
PubMed: 28539509
Affiliations:
- France, États-Unis
- Colorado, Géorgie (États-Unis), Languedoc-Roussillon, Occitanie (région administrative)
- Banyuls-sur-Mer
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Tulenko</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144</wicri:regionArea><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author><author><name sortKey="Massey, James L" sort="Massey, James L" uniqKey="Massey J" first="James L" last="Massey">James L. Massey</name><affiliation wicri:level="2"><nlm:affiliation>Department of Ecology and Evolutionary Biology, University of Colorado Boulder, CO 80309, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Ecology and Evolutionary Biology, University of Colorado Boulder, CO 80309</wicri:regionArea><placeName><region type="state">Colorado</region></placeName></affiliation></author><author><name sortKey="Holmquist, Elishka" sort="Holmquist, Elishka" uniqKey="Holmquist E" first="Elishka" last="Holmquist">Elishka Holmquist</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144</wicri:regionArea><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author><author><name sortKey="Kigundu, Gabriel" sort="Kigundu, Gabriel" uniqKey="Kigundu G" first="Gabriel" last="Kigundu">Gabriel Kigundu</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144</wicri:regionArea><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author><author><name sortKey="Thomas, Sarah" sort="Thomas, Sarah" uniqKey="Thomas S" first="Sarah" last="Thomas">Sarah Thomas</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144</wicri:regionArea><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author><author><name sortKey="Smith, Susan M E" sort="Smith, Susan M E" uniqKey="Smith S" first="Susan M E" last="Smith">Susan M E. Smith</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144</wicri:regionArea><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author><author><name sortKey="Mazan, Sylvie" sort="Mazan, Sylvie" uniqKey="Mazan S" first="Sylvie" last="Mazan">Sylvie Mazan</name><affiliation wicri:level="3"><nlm:affiliation>CNRS, Sorbonne Universités, UPMC Univ Paris 06, UMR7232, Observatoire Océanologique, F-66650 Banyuls-sur-Mer, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>CNRS, Sorbonne Universités, UPMC Univ Paris 06, UMR7232, Observatoire Océanologique, F-66650 Banyuls-sur-Mer</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Banyuls-sur-Mer</settlement></placeName></affiliation></author><author><name sortKey="Davis, Marcus C" sort="Davis, Marcus C" uniqKey="Davis M" first="Marcus C" last="Davis">Marcus C. Davis</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144, USA mdavi144@kennesaw.edu.</nlm:affiliation><country wicri:rule="url">États-Unis</country><wicri:regionArea>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144</wicri:regionArea><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author></analytic><series><title level="j">Proceedings. Biological sciences</title><idno type="eISSN">1471-2954</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The evolutionary origin of the autopod involved a loss of the fin-fold and associated dermal skeleton with a concomitant elaboration of the distal endoskeleton to form a wrist and digits. Developmental studies, primarily from teleosts and amniotes, suggest a model for appendage evolution in which a delay in the AER-to-fin-fold conversion fuelled endoskeletal expansion by prolonging the function of AER-mediated regulatory networks. Here, we characterize aspects of paired fin development in the paddlefish Polyodon spathula (a non-teleost actinopterygian) and catshark Scyliorhinus canicula (chondrichthyan) to explore aspects of this model in a broader phylogenetic context. Our data demonstrate that in basal gnathostomes, the autopod marker HoxA13 co-localizes with the dermoskeleton component And1 to mark the position of the fin-fold, supporting recent work demonstrating a role for HoxA13 in zebrafish fin ray development. Additionally, we show that in paddlefish, the proximal fin and fin-fold mesenchyme share a common mesodermal origin, and that components of the Shh/LIM/Gremlin/Fgf transcriptional network critical to limb bud outgrowth and patterning are expressed in the fin-fold with a profile similar to that of tetrapods. Together these data draw contrast with hypotheses of AER heterochrony and suggest that limb-specific morphologies arose through evolutionary changes in the differentiation outcome of conserved early distal patterning compartments.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">28539509</PMID><DateCreated><Year>2017</Year><Month>05</Month><Day>25</Day></DateCreated><DateRevised><Year>2017</Year><Month>06</Month><Day>06</Day></DateRevised><Article PubModel="Print"><Journal><ISSN IssnType="Electronic">1471-2954</ISSN><JournalIssue CitedMedium="Internet"><Volume>284</Volume><Issue>1855</Issue><PubDate><Year>2017</Year><Month>May</Month><Day>31</Day></PubDate></JournalIssue><Title>Proceedings. Biological sciences</Title><ISOAbbreviation>Proc. Biol. Sci.</ISOAbbreviation></Journal><ArticleTitle>Fin-fold development in paddlefish and catshark and implications for the evolution of the autopod.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">20162780</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1098/rspb.2016.2780</ELocationID><Abstract><AbstractText>The evolutionary origin of the autopod involved a loss of the fin-fold and associated dermal skeleton with a concomitant elaboration of the distal endoskeleton to form a wrist and digits. Developmental studies, primarily from teleosts and amniotes, suggest a model for appendage evolution in which a delay in the AER-to-fin-fold conversion fuelled endoskeletal expansion by prolonging the function of AER-mediated regulatory networks. Here, we characterize aspects of paired fin development in the paddlefish Polyodon spathula (a non-teleost actinopterygian) and catshark Scyliorhinus canicula (chondrichthyan) to explore aspects of this model in a broader phylogenetic context. Our data demonstrate that in basal gnathostomes, the autopod marker HoxA13 co-localizes with the dermoskeleton component And1 to mark the position of the fin-fold, supporting recent work demonstrating a role for HoxA13 in zebrafish fin ray development. Additionally, we show that in paddlefish, the proximal fin and fin-fold mesenchyme share a common mesodermal origin, and that components of the Shh/LIM/Gremlin/Fgf transcriptional network critical to limb bud outgrowth and patterning are expressed in the fin-fold with a profile similar to that of tetrapods. Together these data draw contrast with hypotheses of AER heterochrony and suggest that limb-specific morphologies arose through evolutionary changes in the differentiation outcome of conserved early distal patterning compartments.</AbstractText><CopyrightInformation>© 2017 The Author(s).</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Tulenko</LastName><ForeName>Frank J</ForeName><Initials>FJ</Initials><Identifier Source="ORCID">http://orcid.org/0000-0003-3142-3551</Identifier><AffiliationInfo><Affiliation>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Australian Regenerative Medicine Institute, Monash University, Victoria, 3800, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Massey</LastName><ForeName>James L</ForeName><Initials>JL</Initials><AffiliationInfo><Affiliation>Department of Ecology and Evolutionary Biology, University of Colorado Boulder, CO 80309, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Holmquist</LastName><ForeName>Elishka</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kigundu</LastName><ForeName>Gabriel</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Thomas</LastName><ForeName>Sarah</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Smith</LastName><ForeName>Susan M E</ForeName><Initials>SME</Initials><AffiliationInfo><Affiliation>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mazan</LastName><ForeName>Sylvie</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>CNRS, Sorbonne Universités, UPMC Univ Paris 06, UMR7232, Observatoire Océanologique, F-66650 Banyuls-sur-Mer, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Davis</LastName><ForeName>Marcus C</ForeName><Initials>MC</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-2462-0138</Identifier><AffiliationInfo><Affiliation>Department of Molecular and Cellular Biology, Kennesaw State University, GA 30144, USA mdavi144@kennesaw.edu.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Proc Biol Sci</MedlineTA><NlmUniqueID>101245157</NlmUniqueID><ISSNLinking>0962-8452</ISSNLinking></MedlineJournalInfo><CommentsCorrectionsList><CommentsCorrections RefType="Cites"><RefSource>Nat Commun. 2016 May 23;7:11582</RefSource><PMID Version="1">27211489</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Elife. 2015 Aug 18;4:null</RefSource><PMID Version="1">26283004</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Science. 2014 Aug 1;345(6196):566-70</RefSource><PMID Version="1">25082703</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Nature. 2002 Apr 4;416(6880):527-31</RefSource><PMID Version="1">11932743</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Development. 2014 Apr;141(7):1534-43</RefSource><PMID 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PubStatus="pmc-release"><Year>2018</Year><Month>05</Month><Day>31</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2017</Year><Month>5</Month><Day>26</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2017</Year><Month>5</Month><Day>26</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2017</Year><Month>5</Month><Day>26</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">28539509</ArticleId><ArticleId IdType="pii">rspb.2016.2780</ArticleId><ArticleId IdType="doi">10.1098/rspb.2016.2780</ArticleId><ArticleId IdType="pmc">PMC5454254</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>France</li><li>États-Unis</li></country><region><li>Colorado</li><li>Géorgie (États-Unis)</li><li>Languedoc-Roussillon</li><li>Occitanie (région administrative)</li></region><settlement><li>Banyuls-sur-Mer</li></settlement></list><tree><country name="États-Unis"><region name="Géorgie (États-Unis)"><name sortKey="Tulenko, Frank J" sort="Tulenko, Frank J" uniqKey="Tulenko F" first="Frank J" last="Tulenko">Frank J. Tulenko</name></region><name sortKey="Davis, Marcus C" sort="Davis, Marcus C" uniqKey="Davis M" first="Marcus C" last="Davis">Marcus C. Davis</name><name sortKey="Holmquist, Elishka" sort="Holmquist, Elishka" uniqKey="Holmquist E" first="Elishka" last="Holmquist">Elishka Holmquist</name><name sortKey="Kigundu, Gabriel" sort="Kigundu, Gabriel" uniqKey="Kigundu G" first="Gabriel" last="Kigundu">Gabriel Kigundu</name><name sortKey="Massey, James L" sort="Massey, James L" uniqKey="Massey J" first="James L" last="Massey">James L. Massey</name><name sortKey="Smith, Susan M E" sort="Smith, Susan M E" uniqKey="Smith S" first="Susan M E" last="Smith">Susan M E. Smith</name><name sortKey="Thomas, Sarah" sort="Thomas, Sarah" uniqKey="Thomas S" first="Sarah" last="Thomas">Sarah Thomas</name></country><country name="France"><region name="Occitanie (région administrative)"><name sortKey="Mazan, Sylvie" sort="Mazan, Sylvie" uniqKey="Mazan S" first="Sylvie" last="Mazan">Sylvie Mazan</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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