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Evolutionary Genomics and Adaptive Evolution of the Hedgehog Gene Family (Shh, Ihh and Dhh) in Vertebrates

The Hedgehog (Hh) gene family codes for a class of secreted proteins composed of two active domains that act as signalling molecules during embryo development, namely for the development of the nervous and skeletal systems and the formation of the testis cord. While only one Hh gene is found typical...

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Autores principales: Pereira, Joana, Johnson, Warren E., O’Brien, Stephen J., Jarvis, Erich D., Zhang, Guojie, Gilbert, M. Thomas P., Vasconcelos, Vitor, Antunes, Agostinho
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4280113/
https://www.ncbi.nlm.nih.gov/pubmed/25549322
http://dx.doi.org/10.1371/journal.pone.0074132
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author Pereira, Joana
Johnson, Warren E.
O’Brien, Stephen J.
Jarvis, Erich D.
Zhang, Guojie
Gilbert, M. Thomas P.
Vasconcelos, Vitor
Antunes, Agostinho
author_facet Pereira, Joana
Johnson, Warren E.
O’Brien, Stephen J.
Jarvis, Erich D.
Zhang, Guojie
Gilbert, M. Thomas P.
Vasconcelos, Vitor
Antunes, Agostinho
author_sort Pereira, Joana
collection PubMed
description The Hedgehog (Hh) gene family codes for a class of secreted proteins composed of two active domains that act as signalling molecules during embryo development, namely for the development of the nervous and skeletal systems and the formation of the testis cord. While only one Hh gene is found typically in invertebrate genomes, most vertebrates species have three (Sonic hedgehog – Shh; Indian hedgehog – Ihh; and Desert hedgehog – Dhh), each with different expression patterns and functions, which likely helped promote the increasing complexity of vertebrates and their successful diversification. In this study, we used comparative genomic and adaptive evolutionary analyses to characterize the evolution of the Hh genes in vertebrates following the two major whole genome duplication (WGD) events. To overcome the lack of Hh-coding sequences on avian publicly available databases, we used an extensive dataset of 45 avian and three non-avian reptilian genomes to show that birds have all three Hh paralogs. We find suggestions that following the WGD events, vertebrate Hh paralogous genes evolved independently within similar linkage groups and under different evolutionary rates, especially within the catalytic domain. The structural regions around the ion-binding site were identified to be under positive selection in the signaling domain. These findings contrast with those observed in invertebrates, where different lineages that experienced gene duplication retained similar selective constraints in the Hh orthologs. Our results provide new insights on the evolutionary history of the Hh gene family, the functional roles of these paralogs in vertebrate species, and on the location of mutational hotspots.
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spelling pubmed-42801132015-01-07 Evolutionary Genomics and Adaptive Evolution of the Hedgehog Gene Family (Shh, Ihh and Dhh) in Vertebrates Pereira, Joana Johnson, Warren E. O’Brien, Stephen J. Jarvis, Erich D. Zhang, Guojie Gilbert, M. Thomas P. Vasconcelos, Vitor Antunes, Agostinho PLoS One Research Article The Hedgehog (Hh) gene family codes for a class of secreted proteins composed of two active domains that act as signalling molecules during embryo development, namely for the development of the nervous and skeletal systems and the formation of the testis cord. While only one Hh gene is found typically in invertebrate genomes, most vertebrates species have three (Sonic hedgehog – Shh; Indian hedgehog – Ihh; and Desert hedgehog – Dhh), each with different expression patterns and functions, which likely helped promote the increasing complexity of vertebrates and their successful diversification. In this study, we used comparative genomic and adaptive evolutionary analyses to characterize the evolution of the Hh genes in vertebrates following the two major whole genome duplication (WGD) events. To overcome the lack of Hh-coding sequences on avian publicly available databases, we used an extensive dataset of 45 avian and three non-avian reptilian genomes to show that birds have all three Hh paralogs. We find suggestions that following the WGD events, vertebrate Hh paralogous genes evolved independently within similar linkage groups and under different evolutionary rates, especially within the catalytic domain. The structural regions around the ion-binding site were identified to be under positive selection in the signaling domain. These findings contrast with those observed in invertebrates, where different lineages that experienced gene duplication retained similar selective constraints in the Hh orthologs. Our results provide new insights on the evolutionary history of the Hh gene family, the functional roles of these paralogs in vertebrate species, and on the location of mutational hotspots. Public Library of Science 2014-12-30 /pmc/articles/PMC4280113/ /pubmed/25549322 http://dx.doi.org/10.1371/journal.pone.0074132 Text en © 2014 Pereira et al http://creativecommons.org/licenses/by/4.0/ 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 author and source are properly credited.
spellingShingle Research Article
Pereira, Joana
Johnson, Warren E.
O’Brien, Stephen J.
Jarvis, Erich D.
Zhang, Guojie
Gilbert, M. Thomas P.
Vasconcelos, Vitor
Antunes, Agostinho
Evolutionary Genomics and Adaptive Evolution of the Hedgehog Gene Family (Shh, Ihh and Dhh) in Vertebrates
title Evolutionary Genomics and Adaptive Evolution of the Hedgehog Gene Family (Shh, Ihh and Dhh) in Vertebrates
title_full Evolutionary Genomics and Adaptive Evolution of the Hedgehog Gene Family (Shh, Ihh and Dhh) in Vertebrates
title_fullStr Evolutionary Genomics and Adaptive Evolution of the Hedgehog Gene Family (Shh, Ihh and Dhh) in Vertebrates
title_full_unstemmed Evolutionary Genomics and Adaptive Evolution of the Hedgehog Gene Family (Shh, Ihh and Dhh) in Vertebrates
title_short Evolutionary Genomics and Adaptive Evolution of the Hedgehog Gene Family (Shh, Ihh and Dhh) in Vertebrates
title_sort evolutionary genomics and adaptive evolution of the hedgehog gene family (shh, ihh and dhh) in vertebrates
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4280113/
https://www.ncbi.nlm.nih.gov/pubmed/25549322
http://dx.doi.org/10.1371/journal.pone.0074132
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