Cargando…

A median fin derived from the lateral plate mesoderm and the origin of paired fins

The development of paired appendages was a key innovation during evolution and facilitated the aquatic to terrestrial transition of vertebrates. Largely derived from the lateral plate mesoderm (LPM), one hypothesis for the evolution of paired fins invokes derivation from unpaired median fins via a p...

Descripción completa

Detalles Bibliográficos
Autores principales: Tzung, Keh-Weei, Lalonde, Robert L., Prummel, Karin D., Mahabaleshwar, Harsha, Moran, Hannah R., Stundl, Jan, Cass, Amanda N., Le, Yao, Lea, Robert, Dorey, Karel, Tomecka, Monika J., Zhang, Changqing, Brombacher, Eline C., White, William T., Roehl, Henry H., Tulenko, Frank J., Winkler, Christoph, Currie, Peter D., Amaya, Enrique, Davis, Marcus C., Bronner, Marianne E., Mosimann, Christian, Carney, Tom J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10266977/
https://www.ncbi.nlm.nih.gov/pubmed/37225983
http://dx.doi.org/10.1038/s41586-023-06100-w
_version_ 1785058847139823616
author Tzung, Keh-Weei
Lalonde, Robert L.
Prummel, Karin D.
Mahabaleshwar, Harsha
Moran, Hannah R.
Stundl, Jan
Cass, Amanda N.
Le, Yao
Lea, Robert
Dorey, Karel
Tomecka, Monika J.
Zhang, Changqing
Brombacher, Eline C.
White, William T.
Roehl, Henry H.
Tulenko, Frank J.
Winkler, Christoph
Currie, Peter D.
Amaya, Enrique
Davis, Marcus C.
Bronner, Marianne E.
Mosimann, Christian
Carney, Tom J.
author_facet Tzung, Keh-Weei
Lalonde, Robert L.
Prummel, Karin D.
Mahabaleshwar, Harsha
Moran, Hannah R.
Stundl, Jan
Cass, Amanda N.
Le, Yao
Lea, Robert
Dorey, Karel
Tomecka, Monika J.
Zhang, Changqing
Brombacher, Eline C.
White, William T.
Roehl, Henry H.
Tulenko, Frank J.
Winkler, Christoph
Currie, Peter D.
Amaya, Enrique
Davis, Marcus C.
Bronner, Marianne E.
Mosimann, Christian
Carney, Tom J.
author_sort Tzung, Keh-Weei
collection PubMed
description The development of paired appendages was a key innovation during evolution and facilitated the aquatic to terrestrial transition of vertebrates. Largely derived from the lateral plate mesoderm (LPM), one hypothesis for the evolution of paired fins invokes derivation from unpaired median fins via a pair of lateral fin folds located between pectoral and pelvic fin territories(1). Whilst unpaired and paired fins exhibit similar structural and molecular characteristics, no definitive evidence exists for paired lateral fin folds in larvae or adults of any extant or extinct species. As unpaired fin core components are regarded as exclusively derived from paraxial mesoderm, any transition presumes both co-option of a fin developmental programme to the LPM and bilateral duplication(2). Here, we identify that the larval zebrafish unpaired pre-anal fin fold (PAFF) is derived from the LPM and thus may represent a developmental intermediate between median and paired fins. We trace the contribution of LPM to the PAFF in both cyclostomes and gnathostomes, supporting the notion that this is an ancient trait of vertebrates. Finally, we observe that the PAFF can be bifurcated by increasing bone morphogenetic protein signalling, generating LPM-derived paired fin folds. Our work provides evidence that lateral fin folds may have existed as embryonic anlage for elaboration to paired fins.
format Online
Article
Text
id pubmed-10266977
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-102669772023-06-15 A median fin derived from the lateral plate mesoderm and the origin of paired fins Tzung, Keh-Weei Lalonde, Robert L. Prummel, Karin D. Mahabaleshwar, Harsha Moran, Hannah R. Stundl, Jan Cass, Amanda N. Le, Yao Lea, Robert Dorey, Karel Tomecka, Monika J. Zhang, Changqing Brombacher, Eline C. White, William T. Roehl, Henry H. Tulenko, Frank J. Winkler, Christoph Currie, Peter D. Amaya, Enrique Davis, Marcus C. Bronner, Marianne E. Mosimann, Christian Carney, Tom J. Nature Article The development of paired appendages was a key innovation during evolution and facilitated the aquatic to terrestrial transition of vertebrates. Largely derived from the lateral plate mesoderm (LPM), one hypothesis for the evolution of paired fins invokes derivation from unpaired median fins via a pair of lateral fin folds located between pectoral and pelvic fin territories(1). Whilst unpaired and paired fins exhibit similar structural and molecular characteristics, no definitive evidence exists for paired lateral fin folds in larvae or adults of any extant or extinct species. As unpaired fin core components are regarded as exclusively derived from paraxial mesoderm, any transition presumes both co-option of a fin developmental programme to the LPM and bilateral duplication(2). Here, we identify that the larval zebrafish unpaired pre-anal fin fold (PAFF) is derived from the LPM and thus may represent a developmental intermediate between median and paired fins. We trace the contribution of LPM to the PAFF in both cyclostomes and gnathostomes, supporting the notion that this is an ancient trait of vertebrates. Finally, we observe that the PAFF can be bifurcated by increasing bone morphogenetic protein signalling, generating LPM-derived paired fin folds. Our work provides evidence that lateral fin folds may have existed as embryonic anlage for elaboration to paired fins. Nature Publishing Group UK 2023-05-24 2023 /pmc/articles/PMC10266977/ /pubmed/37225983 http://dx.doi.org/10.1038/s41586-023-06100-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Tzung, Keh-Weei
Lalonde, Robert L.
Prummel, Karin D.
Mahabaleshwar, Harsha
Moran, Hannah R.
Stundl, Jan
Cass, Amanda N.
Le, Yao
Lea, Robert
Dorey, Karel
Tomecka, Monika J.
Zhang, Changqing
Brombacher, Eline C.
White, William T.
Roehl, Henry H.
Tulenko, Frank J.
Winkler, Christoph
Currie, Peter D.
Amaya, Enrique
Davis, Marcus C.
Bronner, Marianne E.
Mosimann, Christian
Carney, Tom J.
A median fin derived from the lateral plate mesoderm and the origin of paired fins
title A median fin derived from the lateral plate mesoderm and the origin of paired fins
title_full A median fin derived from the lateral plate mesoderm and the origin of paired fins
title_fullStr A median fin derived from the lateral plate mesoderm and the origin of paired fins
title_full_unstemmed A median fin derived from the lateral plate mesoderm and the origin of paired fins
title_short A median fin derived from the lateral plate mesoderm and the origin of paired fins
title_sort median fin derived from the lateral plate mesoderm and the origin of paired fins
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10266977/
https://www.ncbi.nlm.nih.gov/pubmed/37225983
http://dx.doi.org/10.1038/s41586-023-06100-w
work_keys_str_mv AT tzungkehweei amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT lalonderobertl amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT prummelkarind amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT mahabaleshwarharsha amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT moranhannahr amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT stundljan amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT cassamandan amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT leyao amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT learobert amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT doreykarel amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT tomeckamonikaj amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT zhangchangqing amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT brombacherelinec amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT whitewilliamt amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT roehlhenryh amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT tulenkofrankj amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT winklerchristoph amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT curriepeterd amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT amayaenrique amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT davismarcusc amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT bronnermariannee amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT mosimannchristian amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT carneytomj amedianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT tzungkehweei medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT lalonderobertl medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT prummelkarind medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT mahabaleshwarharsha medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT moranhannahr medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT stundljan medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT cassamandan medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT leyao medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT learobert medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT doreykarel medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT tomeckamonikaj medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT zhangchangqing medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT brombacherelinec medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT whitewilliamt medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT roehlhenryh medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT tulenkofrankj medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT winklerchristoph medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT curriepeterd medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT amayaenrique medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT davismarcusc medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT bronnermariannee medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT mosimannchristian medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins
AT carneytomj medianfinderivedfromthelateralplatemesodermandtheoriginofpairedfins