A new mechanistic scenario for the origin and evolution of vertebrate cartilage.

The appearance of cellular cartilage was a defining event in vertebrate evolution because it made possible the physical expansion of the vertebrate "new head". Despite its central role in vertebrate evolution, the origin of cellular cartilage has been difficult to understand. This is large...

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Autores principales:	Maria Cattell, Su Lai, Robert Cerny, Daniel Meulemans Medeiros
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2011
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/d5f22efd0bde48bf9685bf9cb15b293e
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spelling	oai:doaj.org-article:d5f22efd0bde48bf9685bf9cb15b293e2021-11-18T06:49:36ZA new mechanistic scenario for the origin and evolution of vertebrate cartilage.1932-620310.1371/journal.pone.0022474https://doaj.org/article/d5f22efd0bde48bf9685bf9cb15b293e2011-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21799866/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203The appearance of cellular cartilage was a defining event in vertebrate evolution because it made possible the physical expansion of the vertebrate "new head". Despite its central role in vertebrate evolution, the origin of cellular cartilage has been difficult to understand. This is largely due to a lack of informative evolutionary intermediates linking vertebrate cellular cartilage to the acellular cartilage of invertebrate chordates. The basal jawless vertebrate, lamprey, has long been considered key to understanding the evolution of vertebrate cartilage. However, histological analyses of the lamprey head skeleton suggest it is composed of modern cellular cartilage and a putatively unrelated connective tissue called mucocartilage, with no obvious transitional tissue. Here we take a molecular approach to better understand the evolutionary relationships between lamprey cellular cartilage, gnathostome cellular cartilage, and lamprey mucocartilage. We find that despite overt histological similarity, lamprey and gnathostome cellular cartilage utilize divergent gene regulatory networks (GRNs). While the gnathostome cellular cartilage GRN broadly incorporates Runx, Barx, and Alx transcription factors, lamprey cellular cartilage does not express Runx or Barx, and only deploys Alx genes in certain regions. Furthermore, we find that lamprey mucocartilage, despite its distinctive mesenchymal morphology, deploys every component of the gnathostome cartilage GRN, albeit in different domains. Based on these findings, and previous work, we propose a stepwise model for the evolution of vertebrate cellular cartilage in which the appearance of a generic neural crest-derived skeletal tissue was followed by a phase of skeletal tissue diversification in early agnathans. In the gnathostome lineage, a single type of rigid cellular cartilage became dominant, replacing other skeletal tissues and evolving via gene cooption to become the definitive cellular cartilage of modern jawed vertebrates.Maria CattellSu LaiRobert CernyDaniel Meulemans MedeirosPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 6, Iss 7, p e22474 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Maria Cattell Su Lai Robert Cerny Daniel Meulemans Medeiros A new mechanistic scenario for the origin and evolution of vertebrate cartilage.
description	The appearance of cellular cartilage was a defining event in vertebrate evolution because it made possible the physical expansion of the vertebrate "new head". Despite its central role in vertebrate evolution, the origin of cellular cartilage has been difficult to understand. This is largely due to a lack of informative evolutionary intermediates linking vertebrate cellular cartilage to the acellular cartilage of invertebrate chordates. The basal jawless vertebrate, lamprey, has long been considered key to understanding the evolution of vertebrate cartilage. However, histological analyses of the lamprey head skeleton suggest it is composed of modern cellular cartilage and a putatively unrelated connective tissue called mucocartilage, with no obvious transitional tissue. Here we take a molecular approach to better understand the evolutionary relationships between lamprey cellular cartilage, gnathostome cellular cartilage, and lamprey mucocartilage. We find that despite overt histological similarity, lamprey and gnathostome cellular cartilage utilize divergent gene regulatory networks (GRNs). While the gnathostome cellular cartilage GRN broadly incorporates Runx, Barx, and Alx transcription factors, lamprey cellular cartilage does not express Runx or Barx, and only deploys Alx genes in certain regions. Furthermore, we find that lamprey mucocartilage, despite its distinctive mesenchymal morphology, deploys every component of the gnathostome cartilage GRN, albeit in different domains. Based on these findings, and previous work, we propose a stepwise model for the evolution of vertebrate cellular cartilage in which the appearance of a generic neural crest-derived skeletal tissue was followed by a phase of skeletal tissue diversification in early agnathans. In the gnathostome lineage, a single type of rigid cellular cartilage became dominant, replacing other skeletal tissues and evolving via gene cooption to become the definitive cellular cartilage of modern jawed vertebrates.
format	article
author	Maria Cattell Su Lai Robert Cerny Daniel Meulemans Medeiros
author_facet	Maria Cattell Su Lai Robert Cerny Daniel Meulemans Medeiros
author_sort	Maria Cattell
title	A new mechanistic scenario for the origin and evolution of vertebrate cartilage.
title_short	A new mechanistic scenario for the origin and evolution of vertebrate cartilage.
title_full	A new mechanistic scenario for the origin and evolution of vertebrate cartilage.
title_fullStr	A new mechanistic scenario for the origin and evolution of vertebrate cartilage.
title_full_unstemmed	A new mechanistic scenario for the origin and evolution of vertebrate cartilage.
title_sort	new mechanistic scenario for the origin and evolution of vertebrate cartilage.
publisher	Public Library of Science (PLoS)
publishDate	2011
url	https://doaj.org/article/d5f22efd0bde48bf9685bf9cb15b293e
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A new mechanistic scenario for the origin and evolution of vertebrate cartilage.

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