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Gene rearrangements in gekkonid mitochondrial genomes with shuffling, loss, and reassignment of tRNA genes.

ABSTRACT: BACKGROUND:Vertebrate mitochondrial genomes (mitogenomes) are 16-18 kbp double-stranded circular DNAs that encode a set of 37 genes. The arrangement of these genes and the major noncoding region is relatively conserved through evolution although gene rearrangements have been described for diverse lineages. The tandem duplication-random loss model has been invoked to explain the mechanisms of most mitochondrial gene rearrangements. Previously reported mitogenomic sequences for geckos rarely included gene rearrangements, which we explore in the present study. RESULTS:We determined seven new mitogenomic sequences from Gekkonidae using a high-throughput sequencing method. The Tropiocolotes tripolitanus mitogenome involves a tandem duplication of the gene block: tRNAArg, NADH dehydrogenase subunit 4L, and NADH dehydrogenase subunit 4. One of the duplicate copies for each protein-coding gene may be pseudogenized. A duplicate copy of the tRNAArg gene appears to have been converted to a tRNAGln gene by a C to T base substitution at the second anticodon position, although this gene may not be fully functional in protein synthesis. The Stenodactylus petrii mitogenome includes several tandem duplications of tRNALeu genes, as well as a translocation of the tRNAAla gene and a putative origin of light-strand replication within a tRNA gene cluster. Finally, the Uroplatus fimbriatus and U. ebenaui mitogenomes feature the apparent loss of the tRNAGlu gene from its original position. Uroplatus fimbriatus appears to retain a translocated tRNAGlu gene adjacent to the 5' end of the major noncoding region. CONCLUSIONS:The present study describes several new mitochondrial gene rearrangements from Gekkonidae. The loss and reassignment of tRNA genes is not very common in vertebrate mitogenomes and our findings raise new questions as to how missing tRNAs are supplied and if the reassigned tRNA gene is fully functional. These new examples of mitochondrial gene rearrangements in geckos should broaden our understanding of the evolution of mitochondrial gene arrangements.

SUBMITTER: Kumazawa Y

PROVIDER: S-EPMC4223735 | biostudies-literature | 2014 Oct

REPOSITORIES: biostudies-literature

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Gene rearrangements in gekkonid mitochondrial genomes with shuffling, loss, and reassignment of tRNA genes.

Kumazawa Yoshinori Y Miura Saaya S Yamada Chiemi C Hashiguchi Yasuyuki Y

BMC genomics 20141024

<h4>Background</h4>Vertebrate mitochondrial genomes (mitogenomes) are 16-18 kbp double-stranded circular DNAs that encode a set of 37 genes. The arrangement of these genes and the major noncoding region is relatively conserved through evolution although gene rearrangements have been described for diverse lineages. The tandem duplication-random loss model has been invoked to explain the mechanisms of most mitochondrial gene rearrangements. Previously reported mitogenomic sequences for geckos rare ...[more]

PMID: 25344428

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Project description:BackgroundRecent mitochondrial phylogenomics studies have reported a sister-group relationship of the orders Capsalidea and Dactylogyridea, which is inconsistent with previous morphology- and molecular-based phylogenies. As Dactylogyridea mitochondrial genomes (mitogenomes) are currently represented by only one family, to improve the phylogenetic resolution, we sequenced and characterized two dactylogyridean parasites, Lamellodiscus spari and Lepidotrema longipenis, belonging to a non-represented family Diplectanidae.ResultsThe L. longipenis mitogenome (15,433 bp) contains the standard 36 flatworm mitochondrial genes (atp8 is absent), whereas we failed to detect trnS1, trnC and trnG in L. spari (14,614 bp). Both mitogenomes exhibit unique gene orders (among the Monogenea), with a number of tRNA rearrangements. Both long non-coding regions contain a number of different (partially overlapping) repeat sequences. Intriguingly, these include putative tRNA pseudogenes in a tandem array (17 trnV pseudogenes in L. longipenis, 13 trnY pseudogenes in L. spari). Combined nucleotide diversity, non-synonymous/synonymous substitutions ratio and average sequence identity analyses consistently showed that nad2, nad5 and nad4 were the most variable PCGs, whereas cox1, cox2 and cytb were the most conserved. Phylogenomic analysis showed that the newly sequenced species of the family Diplectanidae formed a sister-group with the Dactylogyridae + Capsalidae clade. Thus Dactylogyridea (represented by the Diplectanidae and Dactylogyridae) was rendered paraphyletic (with high statistical support) by the nested Capsalidea (represented by the Capsalidae) clade.ConclusionsOur results show that nad2, nad5 and nad4 (fast-evolving) would be better candidates than cox1 (slow-evolving) for species identification and population genetics studies in the Diplectanidae. The unique gene order pattern further suggests discontinuous evolution of mitogenomic gene order arrangement in the Class Monogenea. This first report of paraphyly of the Dactylogyridea highlights the need to generate more molecular data for monogenean parasites, in order to be able to clarify their relationships using large datasets, as single-gene markers appear to provide a phylogenetic resolution which is too low for the task.

Project description:BackgroundAcrodonta consists of Agamidae and Chamaeleonidae that have the characteristic acrodont dentition. These two families and Iguanidae sensu lato are members of infraorder Iguania. Phylogenetic relationships and historical biogeography of iguanian lizards still remain to be elucidated in spite of a number of morphological and molecular studies. This issue was addressed by sequencing complete mitochondrial genomes from 10 species that represent major lineages of acrodont lizards. This study also provided a good opportunity to compare molecular evolutionary modes of mitogenomes among different iguanian lineages.ResultsAcrodontan mitogenomes were found to be less conservative than iguanid counterparts with respect to gene arrangement features and rates of sequence evolution. Phylogenetic relationships were constructed with the mitogenomic sequence data and timing of gene rearrangements was inferred on it. The result suggested highly lineage-specific occurrence of several gene rearrangements, except for the translocation of the tRNAPro gene from the 5' to 3' side of the control region, which likely occurred independently in both agamine and chamaeleonid lineages. Phylogenetic analyses strongly suggested the monophyly of Agamidae in relation to Chamaeleonidae and the non-monophyly of traditional genus Chamaeleo within Chamaeleonidae. Uromastyx and Brookesia were suggested to be the earliest shoot-off of Agamidae and Chamaeleonidae, respectively. Together with the results of relaxed-clock dating analyses, our molecular phylogeny was used to infer the origin of Acrodonta and historical biogeography of its descendant lineages. Our molecular data favored Gondwanan origin of Acrodonta, vicariant divergence of Agamidae and Chamaeleonidae in the drifting India-Madagascar landmass, and migration of the Agamidae to Eurasia with the Indian subcontinent, although Laurasian origin of Acrodonta was not strictly ruled out.ConclusionsWe detected distinct modes of mitogenomic evolution among iguanian families. Agamidae was highlighted in including a number of lineage-specific mitochondrial gene rearrangements. The mitogenomic data provided a certain level of resolution in reconstructing acrodontan phylogeny, although there still remain ambiguous relationships. Our biogeographic implications shed a light on the previous hypothesis of Gondwanan origin of Acrodonta by adding some new evidence and concreteness.

Dataset Information

Gene rearrangements in gekkonid mitochondrial genomes with shuffling, loss, and reassignment of tRNA genes.

Publications

Gene rearrangements in gekkonid mitochondrial genomes with shuffling, loss, and reassignment of tRNA genes.

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