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

ABSTRACT: 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.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 (?HoxD12). 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.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.

SUBMITTER: Wu R

PROVIDER: S-EPMC4470032 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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

Wu Riga R Liu Qingfeng Q Meng Shaoquan S Zhang Peng P Liang Dan D

BMC genomics 20150618

<h4>Background</h4>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 ...[more]

PMID: 26084764

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Project description:BackgroundCaecilians (Gymnophiona) are the least speciose extant lissamphibian order, yet living forms capture approximately 250 million years of evolution since their earliest divergences. This long history is reflected in the broad range of skull morphologies exhibited by this largely fossorial, but developmentally diverse, clade. However, this diversity of form makes quantification of caecilian cranial morphology challenging, with highly variable presence or absence of many structures. Consequently, few studies have examined morphological evolution across caecilians. This extensive variation also raises the question of degree of conservation of cranial modules (semi-autonomous subsets of highly-integrated traits) within this clade, allowing us to assess the importance of modular organisation in shaping morphological evolution. We used an intensive surface geometric morphometric approach to quantify cranial morphological variation across all 32 extant caecilian genera. We defined 16 cranial regions using 53 landmarks and 687 curve and 729 surface sliding semilandmarks. With these unprecedented high-dimensional data, we analysed cranial shape and modularity across caecilians assessing phylogenetic, allometric and ecological influences on cranial evolution, as well as investigating the relationships among integration, evolutionary rate, and morphological disparity.ResultsWe found highest support for a ten-module model, with greater integration of the posterior skull. Phylogenetic signal was significant (Kmult?=?0.87, p < 0.01), but stronger in anterior modules, while allometric influences were also significant (R2?=?0.16, p?< 0.01), but stronger posteriorly. Reproductive strategy and degree of fossoriality were small but significant influences on cranial morphology (R2?=?0.03-0.05), after phylogenetic (p?<?0.03) and multiple-test (p?<?0.05) corrections. The quadrate-squamosal 'cheek' module was the fastest evolving module, perhaps due to its pivotal role in the unique dual jaw-closing mechanism of caecilians. Highly integrated modules exhibited both high and low disparities, and no relationship was evident between integration and evolutionary rate.ConclusionsOur high-dimensional approach robustly characterises caecilian cranial evolution and demonstrates that caecilian crania are highly modular and that cranial modules are shaped by differential phylogenetic, allometric, and ecological effects. More broadly, and in contrast to recent studies, this work suggests that there is no simple relationship between integration and evolutionary rate or disparity.

Project description:BackgroundHox genes are key elements in patterning animal development. They are renowned for their, often, clustered organisation in the genome, with supposed mechanistic links between the organisation of the genes and their expression. The widespread distribution and comparable functions of Hox genes across the animals has led to them being a major study system for comparing the molecular bases for construction and divergence of animal morphologies. Echinoderms (including sea urchins, sea stars, sea cucumbers, feather stars and brittle stars) possess one of the most unusual body plans in the animal kingdom with pronounced pentameral symmetry in the adults. Consequently, much interest has focused on their development, evolution and the role of the Hox genes in these processes. In this context, the organisation of echinoderm Hox gene clusters is distinctive. Within the classificatory system of Duboule, echinoderms constitute one of the clearest examples of Disorganized (D) clusters (i.e. intact clusters but with a gene order or orientation rearranged relative to the ancestral state).ResultsHere we describe two Hox genes (Hox11/13d and e) that have been overlooked in most previous work and have not been considered in reconstructions of echinoderm Hox complements and cluster organisation. The two genes are related to Posterior Hox genes and are present in all classes of echinoderm. Importantly, they do not reside in the Hox cluster of any species for which genomic linkage data is available.ConclusionIncorporating the two neglected Posterior Hox genes into assessments of echinoderm Hox gene complements and organisation shows that these animals in fact have Split (S) Hox clusters rather than simply Disorganized (D) clusters within the Duboule classification scheme. This then has implications for how these genes are likely regulated, with them no longer covered by any potential long-range Hox cluster-wide, or multigenic sub-cluster, regulatory mechanisms.

Project description:BackgroundHox gene clusters with at least 13 paralog group (PG) members are common in vertebrate genomes and in that of amphioxus. Ascidians, which belong to the subphylum Tunicata (Urochordata), are phylogenetically positioned between vertebrates and amphioxus, and traditionally divided into two groups: the Pleurogona and the Enterogona. An enterogonan ascidian, Ciona intestinalis (Ci), possesses nine Hox genes localized on two chromosomes; thus, the Hox gene cluster is disintegrated. We investigated the Hox gene cluster of a pleurogonan ascidian, Halocynthia roretzi (Hr) to investigate whether Hox gene cluster disintegration is common among ascidians, and if so, how such disintegration occurred during ascidian or tunicate evolution.ResultsOur phylogenetic analysis reveals that the Hr Hox gene complement comprises nine members, including one with a relatively divergent Hox homeodomain sequence. Eight of nine Hr Hox genes were orthologous to Ci-Hox1, 2, 3, 4, 5, 10, 12 and 13. Following the phylogenetic classification into 13 PGs, we designated Hr Hox genes as Hox1, 2, 3, 4, 5, 10, 11/12/13.a, 11/12/13.b and HoxX. To address the chromosomal arrangement of the nine Hox genes, we performed two-color chromosomal fluorescent in situ hybridization, which revealed that the nine Hox genes are localized on a single chromosome in Hr, distinct from their arrangement in Ci. We further examined the order of the nine Hox genes on the chromosome by chromosome/scaffold walking. This analysis suggested a gene order of Hox1, 11/12/13.b, 11/12/13.a, 10, 5, X, followed by either Hox4, 3, 2 or Hox2, 3, 4 on the chromosome. Based on the present results and those previously reported in Ci, we discuss the establishment of the Hox gene complement and disintegration of Hox gene clusters during the course of ascidian or tunicate evolution.ConclusionsThe Hox gene cluster and the genome must have experienced extensive reorganization during the course of evolution from the ancestral tunicate to Hr and Ci. Nevertheless, some features are shared in Hox gene components and gene arrangement on the chromosomes, suggesting that Hox gene cluster disintegration in ascidians involved early events common to tunicates as well as later ascidian lineage-specific events.

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

Publications

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

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