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Comparative and phylogenomic studies on the mitochondrial genomes of Pentatomomorpha (Insecta: Hemiptera: Heteroptera).

ABSTRACT: BACKGROUND: Nucleotide sequences and the gene arrangements of mitochondrial genomes are effective tools for resolving phylogenetic problems. Hemipteroid insects are known to possess highly reorganized mitochondrial genomes, but in the suborder Heteroptera (Insecta: Hemiptera), there was only one complete mitochondrial genome sequenced without gene rearrangement and the phylogeny of infraorder Pentatomomorpha in Heteroptera was still uncertain. RESULTS: Fifteen mitochondrial genomes of the suborder Heteroptera were sequenced. Gene rearrangements were found as follows: 1) tRNA-I and tRNA-Q switched positions in Aradidae, 2) tRNA-T and tRNA-P switched positions in Largidae and Pyrrhocoridae. Two recombination events were found in Alydidae and Malcidae. The other mt-genomes were organized in the same way as observed in Drosophila yakuba. The phylogenetic analyses of infraorder Pentatomomorpha based on the nucleotide sequence raised the hypothesis of (Aradoidea + (Pentatomoidea + (Pyrrhocoroidea + (Lygaeoidea + Coreoidea)))). The rearrangement of tRNA-T and tRNA-P also linked Largidae and Pyrrhocoridae together. Furthermore, the conserved sequence block in the unusual intergenic spacers between tRNA-H and ND4 favored the monophyly of Lygaeoidea. Tetranucleotide ATCA was inferred to be the initiation codon of ND2 in Cydnidae. No correlation was found between the rates of nucleotide substitution and gene rearrangement. CG content was significantly correlated with the nucleotide substitution rate of each gene. For ND1, there was a positive correlation (P < 0.01) between amino acids variations and hydrophobicity, but a negative correlation (P < 0.01) for ND6. No conserved sequence was found among the control regions and these regions were not always the most AT-rich region of the mt-genome. CONCLUSION: Heteropteran insects are extremely complex groups worthy of further study because of the unusual tetranucleotide initiation codon and their great mt-genomic diversity, including gene rearrangements and recombinations. The mt-genome is a powerful molecular marker for resolving phylogeny at the level of the superfamily and family. Gene rearrangements were not correlated with nucleotide substitution rates. CG content variation caused the different evolutionary patterns among genes. For ND1, in many polar or nonpolar regions the specific identity of the amino acid residues might be more important than maintaining the polarity of these regions, while the opposite is true for ND6. Most sequences of the control regions did not appear to be important for regulatory functions. Finally, we suggest that the term "AT-rich regions" should not be used.

SUBMITTER: Hua J

PROVIDER: S-EPMC2651891 | biostudies-literature | 2008

REPOSITORIES: biostudies-literature

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Comparative and phylogenomic studies on the mitochondrial genomes of Pentatomomorpha (Insecta: Hemiptera: Heteroptera).

Hua Jimeng J Li Ming M Dong Pengzhi P Cui Ying Y Xie Qiang Q Bu Wenjun W

BMC genomics 20081217

<h4>Background</h4>Nucleotide sequences and the gene arrangements of mitochondrial genomes are effective tools for resolving phylogenetic problems. Hemipteroid insects are known to possess highly reorganized mitochondrial genomes, but in the suborder Heteroptera (Insecta: Hemiptera), there was only one complete mitochondrial genome sequenced without gene rearrangement and the phylogeny of infraorder Pentatomomorpha in Heteroptera was still uncertain.<h4>Results</h4>Fifteen mitochondrial genomes ...[more]

PMID: 19091056

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Project description:BackgroundInsect mitochondrial genomes (mitogenomes) are the most extensively used genetic marker for evolutionary and population genetics studies of insects. The Pentatomoidea superfamily is economically important and the largest superfamily within Pentatomomorpha with over 7,000 species. To better understand the diversity and evolution of pentatomoid species, we sequenced and annotated the mitogenomes of Eurydema gebleri and Rubiconia intermedia, and present the first comparative analysis of the 11 pentatomoid mitogenomes that have been sequenced to date.ResultsWe obtained the complete mitogenome of Eurydema gebleri (16,005 bp) and a nearly complete mitogenome of Rubiconia intermedia (14,967 bp). Our results show that gene content, gene arrangement, base composition, codon usage, and mitochondrial transcription termination factor sequences are highly conserved in pentatomoid species, especially for species in the same family. Evolutionary rate analyses of protein-coding genes reveal that the highest and lowest rates are found in atp8 and cox1 and distinctive evolutionary patterns are significantly correlated with the G + C content of genes. We inferred the secondary structures for two rRNA genes for eleven pentatomoid species, and identify some conserved motifs of RNA structures in Pentatomidea. All tRNA genes in pentatomoid mitogenomes have a canonical cloverleaf secondary structure, except for two tRNAs (trnS1 and trnV) which appear to lack the dihydrouridine arm. Regions that are A + T-rich have several distinct characteristics (e.g. size variation and abundant tandem repeats), and have potential as species or population level molecular markers. Phylogenetic analyses based on mitogenomic data strongly support the monophyly of Pentatomoidea, and the estimated phylogenetic relationships are: (Urostylididae + (Plataspidae + (Pentatomidae + (Cydnidae + (Dinidoridae + Tessaratomidae))))).ConclusionsThis comparative mitogenomic analysis sheds light on the architecture and evolution of mitogenomes in the superfamily Pentatomoidea. Mitogenomes can be effectively used to resolve phylogenetic relationships of pentatomomorphan insects at various taxonomic levels. Sequencing more mitogenomes at various taxonomic levels, particularly from closely related species, will improve the annotation accuracy of mitochondrial genes, as well as greatly enhance our understanding of mitogenomic evolution and phylogenetic relationships in pentatomoids.

Dataset Information

Comparative and phylogenomic studies on the mitochondrial genomes of Pentatomomorpha (Insecta: Hemiptera: Heteroptera).

Publications

Comparative and phylogenomic studies on the mitochondrial genomes of Pentatomomorpha (Insecta: Hemiptera: Heteroptera).

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