Heterogeneous conservation of Dlx paralog co-expression in jawed vertebrates.

BACKGROUND: The Dlx gene family encodes transcription factors involved in the development of a wide variety of morphological innovations that first evolved at the origins of vertebrates or of the jawed vertebrates. This gene family expanded with the two rounds of genome duplications that occurred be...

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Main Authors: Mélanie Debiais-Thibaud, Cushla J Metcalfe, Jacob Pollack, Isabelle Germon, Marc Ekker, Michael Depew, Patrick Laurenti, Véronique Borday-Birraux, Didier Casane
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3695995?pdf=render
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spelling doaj-b68128b9ad314cac83c6a71086a22df12020-11-24T21:55:23ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0186e6818210.1371/journal.pone.0068182Heterogeneous conservation of Dlx paralog co-expression in jawed vertebrates.Mélanie Debiais-ThibaudCushla J MetcalfeJacob PollackIsabelle GermonMarc EkkerMichael DepewPatrick LaurentiVéronique Borday-BirrauxDidier CasaneBACKGROUND: The Dlx gene family encodes transcription factors involved in the development of a wide variety of morphological innovations that first evolved at the origins of vertebrates or of the jawed vertebrates. This gene family expanded with the two rounds of genome duplications that occurred before jawed vertebrates diversified. It includes at least three bigene pairs sharing conserved regulatory sequences in tetrapods and teleost fish, but has been only partially characterized in chondrichthyans, the third major group of jawed vertebrates. Here we take advantage of developmental and molecular tools applied to the shark Scyliorhinus canicula to fill in the gap and provide an overview of the evolution of the Dlx family in the jawed vertebrates. These results are analyzed in the theoretical framework of the DDC (Duplication-Degeneration-Complementation) model. RESULTS: The genomic organisation of the catshark Dlx genes is similar to that previously described for tetrapods. Conserved non-coding elements identified in bony fish were also identified in catshark Dlx clusters and showed regulatory activity in transgenic zebrafish. Gene expression patterns in the catshark showed that there are some expression sites with high conservation of the expressed paralog(s) and other expression sites with events of paralog sub-functionalization during jawed vertebrate diversification, resulting in a wide variety of evolutionary scenarios within this gene family. CONCLUSION: Dlx gene expression patterns in the catshark show that there has been little neo-functionalization in Dlx genes over gnathostome evolution. In most cases, one tandem duplication and two rounds of vertebrate genome duplication have led to at least six Dlx coding sequences with redundant expression patterns followed by some instances of paralog sub-functionalization. Regulatory constraints such as shared enhancers, and functional constraints including gene pleiotropy, may have contributed to the evolutionary inertia leading to high redundancy between gene expression patterns.http://europepmc.org/articles/PMC3695995?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Mélanie Debiais-Thibaud
Cushla J Metcalfe
Jacob Pollack
Isabelle Germon
Marc Ekker
Michael Depew
Patrick Laurenti
Véronique Borday-Birraux
Didier Casane
spellingShingle Mélanie Debiais-Thibaud
Cushla J Metcalfe
Jacob Pollack
Isabelle Germon
Marc Ekker
Michael Depew
Patrick Laurenti
Véronique Borday-Birraux
Didier Casane
Heterogeneous conservation of Dlx paralog co-expression in jawed vertebrates.
PLoS ONE
author_facet Mélanie Debiais-Thibaud
Cushla J Metcalfe
Jacob Pollack
Isabelle Germon
Marc Ekker
Michael Depew
Patrick Laurenti
Véronique Borday-Birraux
Didier Casane
author_sort Mélanie Debiais-Thibaud
title Heterogeneous conservation of Dlx paralog co-expression in jawed vertebrates.
title_short Heterogeneous conservation of Dlx paralog co-expression in jawed vertebrates.
title_full Heterogeneous conservation of Dlx paralog co-expression in jawed vertebrates.
title_fullStr Heterogeneous conservation of Dlx paralog co-expression in jawed vertebrates.
title_full_unstemmed Heterogeneous conservation of Dlx paralog co-expression in jawed vertebrates.
title_sort heterogeneous conservation of dlx paralog co-expression in jawed vertebrates.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2013-01-01
description BACKGROUND: The Dlx gene family encodes transcription factors involved in the development of a wide variety of morphological innovations that first evolved at the origins of vertebrates or of the jawed vertebrates. This gene family expanded with the two rounds of genome duplications that occurred before jawed vertebrates diversified. It includes at least three bigene pairs sharing conserved regulatory sequences in tetrapods and teleost fish, but has been only partially characterized in chondrichthyans, the third major group of jawed vertebrates. Here we take advantage of developmental and molecular tools applied to the shark Scyliorhinus canicula to fill in the gap and provide an overview of the evolution of the Dlx family in the jawed vertebrates. These results are analyzed in the theoretical framework of the DDC (Duplication-Degeneration-Complementation) model. RESULTS: The genomic organisation of the catshark Dlx genes is similar to that previously described for tetrapods. Conserved non-coding elements identified in bony fish were also identified in catshark Dlx clusters and showed regulatory activity in transgenic zebrafish. Gene expression patterns in the catshark showed that there are some expression sites with high conservation of the expressed paralog(s) and other expression sites with events of paralog sub-functionalization during jawed vertebrate diversification, resulting in a wide variety of evolutionary scenarios within this gene family. CONCLUSION: Dlx gene expression patterns in the catshark show that there has been little neo-functionalization in Dlx genes over gnathostome evolution. In most cases, one tandem duplication and two rounds of vertebrate genome duplication have led to at least six Dlx coding sequences with redundant expression patterns followed by some instances of paralog sub-functionalization. Regulatory constraints such as shared enhancers, and functional constraints including gene pleiotropy, may have contributed to the evolutionary inertia leading to high redundancy between gene expression patterns.
url http://europepmc.org/articles/PMC3695995?pdf=render
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