Cargando…

Ancient homeobox gene loss and the evolution of chordate brain and pharynx development: deductions from amphioxus gene expression

Homeobox genes encode a large superclass of transcription factors with widespread roles in animal development. Within chordates there are over 100 homeobox genes in the invertebrate cephalochordate amphioxus and over 200 in humans. Set against this general trend of increasing gene number in vertebra...

Descripción completa

Detalles Bibliográficos
Autores principales: Butts, Thomas, Holland, Peter W. H., Ferrier, David E. K.
Formato: Texto
Lenguaje:English
Publicado: The Royal Society 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2982225/
https://www.ncbi.nlm.nih.gov/pubmed/20554554
http://dx.doi.org/10.1098/rspb.2010.0647
_version_ 1782191755012079616
author Butts, Thomas
Holland, Peter W. H.
Ferrier, David E. K.
author_facet Butts, Thomas
Holland, Peter W. H.
Ferrier, David E. K.
author_sort Butts, Thomas
collection PubMed
description Homeobox genes encode a large superclass of transcription factors with widespread roles in animal development. Within chordates there are over 100 homeobox genes in the invertebrate cephalochordate amphioxus and over 200 in humans. Set against this general trend of increasing gene number in vertebrate evolution, some ancient homeobox genes that were present in the last common ancestor of chordates have been lost from vertebrates. Here, we describe the embryonic expression of four amphioxus descendants of these genes—AmphiNedxa, AmphiNedxb, AmphiMsxlx and AmphiNKx7. All four genes are expressed with a striking asymmetry about the left–right axis in the pharyngeal region of neurula embryos, mirroring the pronounced asymmetry of amphioxus embryogenesis. AmphiMsxlx and AmphiNKx7 are also transiently expressed in an anterior neural tube region destined to become the cerebral vesicle. These findings suggest significant rewiring of developmental gene regulatory networks occurred during chordate evolution, coincident with homeobox gene loss. We propose that loss of otherwise widely conserved genes is possible when these genes function in a confined role in development that is subsequently lost or significantly modified during evolution. In the case of these homeobox genes, we propose that this has occurred in relation to the evolution of the chordate pharynx and brain.
format Text
id pubmed-2982225
institution National Center for Biotechnology Information
language English
publishDate 2010
publisher The Royal Society
record_format MEDLINE/PubMed
spelling pubmed-29822252010-11-24 Ancient homeobox gene loss and the evolution of chordate brain and pharynx development: deductions from amphioxus gene expression Butts, Thomas Holland, Peter W. H. Ferrier, David E. K. Proc Biol Sci Research Articles Homeobox genes encode a large superclass of transcription factors with widespread roles in animal development. Within chordates there are over 100 homeobox genes in the invertebrate cephalochordate amphioxus and over 200 in humans. Set against this general trend of increasing gene number in vertebrate evolution, some ancient homeobox genes that were present in the last common ancestor of chordates have been lost from vertebrates. Here, we describe the embryonic expression of four amphioxus descendants of these genes—AmphiNedxa, AmphiNedxb, AmphiMsxlx and AmphiNKx7. All four genes are expressed with a striking asymmetry about the left–right axis in the pharyngeal region of neurula embryos, mirroring the pronounced asymmetry of amphioxus embryogenesis. AmphiMsxlx and AmphiNKx7 are also transiently expressed in an anterior neural tube region destined to become the cerebral vesicle. These findings suggest significant rewiring of developmental gene regulatory networks occurred during chordate evolution, coincident with homeobox gene loss. We propose that loss of otherwise widely conserved genes is possible when these genes function in a confined role in development that is subsequently lost or significantly modified during evolution. In the case of these homeobox genes, we propose that this has occurred in relation to the evolution of the chordate pharynx and brain. The Royal Society 2010-11-22 2010-06-16 /pmc/articles/PMC2982225/ /pubmed/20554554 http://dx.doi.org/10.1098/rspb.2010.0647 Text en © 2010 The Royal Society http://creativecommons.org/licenses/by/2.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Butts, Thomas
Holland, Peter W. H.
Ferrier, David E. K.
Ancient homeobox gene loss and the evolution of chordate brain and pharynx development: deductions from amphioxus gene expression
title Ancient homeobox gene loss and the evolution of chordate brain and pharynx development: deductions from amphioxus gene expression
title_full Ancient homeobox gene loss and the evolution of chordate brain and pharynx development: deductions from amphioxus gene expression
title_fullStr Ancient homeobox gene loss and the evolution of chordate brain and pharynx development: deductions from amphioxus gene expression
title_full_unstemmed Ancient homeobox gene loss and the evolution of chordate brain and pharynx development: deductions from amphioxus gene expression
title_short Ancient homeobox gene loss and the evolution of chordate brain and pharynx development: deductions from amphioxus gene expression
title_sort ancient homeobox gene loss and the evolution of chordate brain and pharynx development: deductions from amphioxus gene expression
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2982225/
https://www.ncbi.nlm.nih.gov/pubmed/20554554
http://dx.doi.org/10.1098/rspb.2010.0647
work_keys_str_mv AT buttsthomas ancienthomeoboxgenelossandtheevolutionofchordatebrainandpharynxdevelopmentdeductionsfromamphioxusgeneexpression
AT hollandpeterwh ancienthomeoboxgenelossandtheevolutionofchordatebrainandpharynxdevelopmentdeductionsfromamphioxusgeneexpression
AT ferrierdavidek ancienthomeoboxgenelossandtheevolutionofchordatebrainandpharynxdevelopmentdeductionsfromamphioxusgeneexpression