Cargando…

Hox cluster characterization of Banna caecilian (Ichthyophis bannanicus) provides hints for slow evolution of its genome

BACKGROUND: Caecilians, with a discrete lifestyle, are the least explored group of amphibians. Though with distinct traits, many aspects of their biology are poorly investigated. Obtaining the caecilian genomic sequences will offer new perspectives and aid the fundamental studies in caecilian biolog...

Descripción completa

Detalles Bibliográficos
Autores principales: Wu, Riga, Liu, Qingfeng, Meng, Shaoquan, Zhang, Peng, Liang, Dan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4470032/
https://www.ncbi.nlm.nih.gov/pubmed/26084764
http://dx.doi.org/10.1186/s12864-015-1684-0
_version_ 1782376691825377280
author Wu, Riga
Liu, Qingfeng
Meng, Shaoquan
Zhang, Peng
Liang, Dan
author_facet Wu, Riga
Liu, Qingfeng
Meng, Shaoquan
Zhang, Peng
Liang, Dan
author_sort Wu, Riga
collection PubMed
description BACKGROUND: Caecilians, with a discrete lifestyle, are the least explored group of amphibians. Though with distinct traits, many aspects of their biology are poorly investigated. Obtaining the caecilian genomic sequences will offer new perspectives and aid the fundamental studies in caecilian biology. The caecilian genomic sequences are also important and practical in the comparative genomics of amphibians. Currently, however, only sparse genomic sequences of caecilians are available. Hox genes, an old family of transcription factors playing central roles in the establishment of metazoan body plan. Understanding their structure and genomic organization may provide insights into the animal’s genome, which is valuable for animals without a sequenced genome. RESULTS: We sequenced and characterized the Hox clusters of Banna caecilian (Ichthyophis bannanicus) with a strategy combining long range PCR and genome walking. We obtained the majority of the four caecilian Hox clusters and identified 39 Hox genes, 5 microRNA genes and 1 pseudogene (ψHoxD12). There remained seven intergenic gaps we were unable to fill. From the obtained sequences, the caecilian Hox clusters contained less repetitive sequences and more conserved noncoding elements (CNEs) than the frog counterparts. We found that caecilian and coelacanth shared many more CNEs than frog and coelacanth did. Relative rate of sequence evolution showed that caecilian Hox genes evolved significantly more slowly than the other tetrapod species used in this study and were comparable to the slowly evolving coelacanth Hox genes. Phylogenetic tree of the four Hox clusters also revealed shorter branch length especially for the caecilian HoxA, HoxB and HoxD clusters. These features of the caecilian Hox clusters suggested a slowly evolving genome, which was supported by further analysis of a large orthologous protein dataset. CONCLUSIONS: Our analyses greatly extended the knowledge about the caecilian Hox clusters from previous PCR surveys. From the obtained Hox sequences and the orthologous protein dataset, the caecilian Hox loci and its genome appear evolving comparatively slowly. As the basal lineage of amphibians and land vertebrate, this characteristic of the caecilian genome is valuable in the study concerning the genome biology and evolution of amphibians and early tetrapods. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1684-0) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4470032
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-44700322015-06-18 Hox cluster characterization of Banna caecilian (Ichthyophis bannanicus) provides hints for slow evolution of its genome Wu, Riga Liu, Qingfeng Meng, Shaoquan Zhang, Peng Liang, Dan BMC Genomics Research Article BACKGROUND: Caecilians, with a discrete lifestyle, are the least explored group of amphibians. Though with distinct traits, many aspects of their biology are poorly investigated. Obtaining the caecilian genomic sequences will offer new perspectives and aid the fundamental studies in caecilian biology. The caecilian genomic sequences are also important and practical in the comparative genomics of amphibians. Currently, however, only sparse genomic sequences of caecilians are available. Hox genes, an old family of transcription factors playing central roles in the establishment of metazoan body plan. Understanding their structure and genomic organization may provide insights into the animal’s genome, which is valuable for animals without a sequenced genome. RESULTS: We sequenced and characterized the Hox clusters of Banna caecilian (Ichthyophis bannanicus) with a strategy combining long range PCR and genome walking. We obtained the majority of the four caecilian Hox clusters and identified 39 Hox genes, 5 microRNA genes and 1 pseudogene (ψHoxD12). There remained seven intergenic gaps we were unable to fill. From the obtained sequences, the caecilian Hox clusters contained less repetitive sequences and more conserved noncoding elements (CNEs) than the frog counterparts. We found that caecilian and coelacanth shared many more CNEs than frog and coelacanth did. Relative rate of sequence evolution showed that caecilian Hox genes evolved significantly more slowly than the other tetrapod species used in this study and were comparable to the slowly evolving coelacanth Hox genes. Phylogenetic tree of the four Hox clusters also revealed shorter branch length especially for the caecilian HoxA, HoxB and HoxD clusters. These features of the caecilian Hox clusters suggested a slowly evolving genome, which was supported by further analysis of a large orthologous protein dataset. CONCLUSIONS: Our analyses greatly extended the knowledge about the caecilian Hox clusters from previous PCR surveys. From the obtained Hox sequences and the orthologous protein dataset, the caecilian Hox loci and its genome appear evolving comparatively slowly. As the basal lineage of amphibians and land vertebrate, this characteristic of the caecilian genome is valuable in the study concerning the genome biology and evolution of amphibians and early tetrapods. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1684-0) contains supplementary material, which is available to authorized users. BioMed Central 2015-06-18 /pmc/articles/PMC4470032/ /pubmed/26084764 http://dx.doi.org/10.1186/s12864-015-1684-0 Text en © Wu et al. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Wu, Riga
Liu, Qingfeng
Meng, Shaoquan
Zhang, Peng
Liang, Dan
Hox cluster characterization of Banna caecilian (Ichthyophis bannanicus) provides hints for slow evolution of its genome
title Hox cluster characterization of Banna caecilian (Ichthyophis bannanicus) provides hints for slow evolution of its genome
title_full Hox cluster characterization of Banna caecilian (Ichthyophis bannanicus) provides hints for slow evolution of its genome
title_fullStr Hox cluster characterization of Banna caecilian (Ichthyophis bannanicus) provides hints for slow evolution of its genome
title_full_unstemmed Hox cluster characterization of Banna caecilian (Ichthyophis bannanicus) provides hints for slow evolution of its genome
title_short Hox cluster characterization of Banna caecilian (Ichthyophis bannanicus) provides hints for slow evolution of its genome
title_sort hox cluster characterization of banna caecilian (ichthyophis bannanicus) provides hints for slow evolution of its genome
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4470032/
https://www.ncbi.nlm.nih.gov/pubmed/26084764
http://dx.doi.org/10.1186/s12864-015-1684-0
work_keys_str_mv AT wuriga hoxclustercharacterizationofbannacaecilianichthyophisbannanicusprovideshintsforslowevolutionofitsgenome
AT liuqingfeng hoxclustercharacterizationofbannacaecilianichthyophisbannanicusprovideshintsforslowevolutionofitsgenome
AT mengshaoquan hoxclustercharacterizationofbannacaecilianichthyophisbannanicusprovideshintsforslowevolutionofitsgenome
AT zhangpeng hoxclustercharacterizationofbannacaecilianichthyophisbannanicusprovideshintsforslowevolutionofitsgenome
AT liangdan hoxclustercharacterizationofbannacaecilianichthyophisbannanicusprovideshintsforslowevolutionofitsgenome