Neofunctionalization in vertebrates: the example of retinoic acid receptors.

Understanding the role of gene duplications in establishing vertebrate innovations is one of the main challenges of Evo-Devo (evolution of development) studies. Data on evolutionary changes in gene expression (i.e., evolution of transcription factor-cis-regulatory elements relationships) tell only p...

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Main Authors: Hector Escriva, Stéphanie Bertrand, Pierre Germain, Marc Robinson-Rechavi, Muriel Umbhauer, Jérôme Cartry, Marilyne Duffraisse, Linda Holland, Hinrich Gronemeyer, Vincent Laudet
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2006-07-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC1500811?pdf=render
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author Hector Escriva
Stéphanie Bertrand
Pierre Germain
Marc Robinson-Rechavi
Muriel Umbhauer
Jérôme Cartry
Marilyne Duffraisse
Linda Holland
Hinrich Gronemeyer
Vincent Laudet
author_facet Hector Escriva
Stéphanie Bertrand
Pierre Germain
Marc Robinson-Rechavi
Muriel Umbhauer
Jérôme Cartry
Marilyne Duffraisse
Linda Holland
Hinrich Gronemeyer
Vincent Laudet
author_sort Hector Escriva
collection DOAJ
description Understanding the role of gene duplications in establishing vertebrate innovations is one of the main challenges of Evo-Devo (evolution of development) studies. Data on evolutionary changes in gene expression (i.e., evolution of transcription factor-cis-regulatory elements relationships) tell only part of the story; protein function, best studied by biochemical and functional assays, can also change. In this study, we have investigated how gene duplication has affected both the expression and the ligand-binding specificity of retinoic acid receptors (RARs), which play a major role in chordate embryonic development. Mammals have three paralogous RAR genes--RAR alpha, beta, and gamma--which resulted from genome duplications at the origin of vertebrates. By using pharmacological ligands selective for specific paralogues, we have studied the ligand-binding capacities of RARs from diverse chordates species. We have found that RAR beta-like binding selectivity is a synapomorphy of all chordate RARs, including a reconstructed synthetic RAR representing the receptor present in the ancestor of chordates. Moreover, comparison of expression patterns of the cephalochordate amphioxus and the vertebrates suggests that, of all the RARs, RAR beta expression has remained most similar to that of the ancestral RAR. On the basis of these results together, we suggest that while RAR beta kept the ancestral RAR role, RAR alpha and RAR gamma diverged both in ligand-binding capacity and in expression patterns. We thus suggest that neofunctionalization occurred at both the expression and the functional levels to shape RAR roles during development in vertebrates.
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spelling doaj.art-6b63d52e77ff4c88a952493a6f502b642022-12-21T19:28:55ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042006-07-0127e10210.1371/journal.pgen.0020102Neofunctionalization in vertebrates: the example of retinoic acid receptors.Hector EscrivaStéphanie BertrandPierre GermainMarc Robinson-RechaviMuriel UmbhauerJérôme CartryMarilyne DuffraisseLinda HollandHinrich GronemeyerVincent LaudetUnderstanding the role of gene duplications in establishing vertebrate innovations is one of the main challenges of Evo-Devo (evolution of development) studies. Data on evolutionary changes in gene expression (i.e., evolution of transcription factor-cis-regulatory elements relationships) tell only part of the story; protein function, best studied by biochemical and functional assays, can also change. In this study, we have investigated how gene duplication has affected both the expression and the ligand-binding specificity of retinoic acid receptors (RARs), which play a major role in chordate embryonic development. Mammals have three paralogous RAR genes--RAR alpha, beta, and gamma--which resulted from genome duplications at the origin of vertebrates. By using pharmacological ligands selective for specific paralogues, we have studied the ligand-binding capacities of RARs from diverse chordates species. We have found that RAR beta-like binding selectivity is a synapomorphy of all chordate RARs, including a reconstructed synthetic RAR representing the receptor present in the ancestor of chordates. Moreover, comparison of expression patterns of the cephalochordate amphioxus and the vertebrates suggests that, of all the RARs, RAR beta expression has remained most similar to that of the ancestral RAR. On the basis of these results together, we suggest that while RAR beta kept the ancestral RAR role, RAR alpha and RAR gamma diverged both in ligand-binding capacity and in expression patterns. We thus suggest that neofunctionalization occurred at both the expression and the functional levels to shape RAR roles during development in vertebrates.http://europepmc.org/articles/PMC1500811?pdf=render
spellingShingle Hector Escriva
Stéphanie Bertrand
Pierre Germain
Marc Robinson-Rechavi
Muriel Umbhauer
Jérôme Cartry
Marilyne Duffraisse
Linda Holland
Hinrich Gronemeyer
Vincent Laudet
Neofunctionalization in vertebrates: the example of retinoic acid receptors.
PLoS Genetics
title Neofunctionalization in vertebrates: the example of retinoic acid receptors.
title_full Neofunctionalization in vertebrates: the example of retinoic acid receptors.
title_fullStr Neofunctionalization in vertebrates: the example of retinoic acid receptors.
title_full_unstemmed Neofunctionalization in vertebrates: the example of retinoic acid receptors.
title_short Neofunctionalization in vertebrates: the example of retinoic acid receptors.
title_sort neofunctionalization in vertebrates the example of retinoic acid receptors
url http://europepmc.org/articles/PMC1500811?pdf=render
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