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

Hua J, Li M, Dong P, Cui Y, Xie Q, Bu W - BMC Genomics (2008)

Bottom Line: Nucleotide sequences and the gene arrangements of mitochondrial genomes are effective tools for resolving phylogenetic problems.Two recombination events were found in Alydidae and Malcidae.Most sequences of the control regions did not appear to be important for regulatory functions.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology and Developmental Biology, Institute of Entomology, College of Life Sciences, Nankai University, Tianjin 300071, PR China. nkhuajimeng@163.com

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.

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Possible evolutionary mechanism of recombination in Alydidae and Malcidae. A, recombination in Alydidae. Panel A.a, the ancestral state. Dup.A1 and Dup.B1 were two original copies of the repetitions. Panel A.b, Dup.A2 and Dup.B2 between tRNA-I and tRNA-Q were repetitions of the Dup.A1 and the Dup.B1 formed by the tandem duplication and random loss. Panel A.c, Dup.A2 changed its direction by intramitochondrial recombination [35], forming the extant state. B, the recombination in Malcidae. Panel B.a, Dup.C1 was the original copy of thr repetition in the intergenic spacer between tRNA-H and ND4. Panel B.b, formation of the mini circle of Dup.C1 by intramitochondrial recombination [35]. Panel B.c, the mini circle of the Dup.C1 integrated into the control region of another mt-genome. Panel B.d, Dup.C2, the repetition of the Dup.C1, formed in the control region.
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Figure 4: Possible evolutionary mechanism of recombination in Alydidae and Malcidae. A, recombination in Alydidae. Panel A.a, the ancestral state. Dup.A1 and Dup.B1 were two original copies of the repetitions. Panel A.b, Dup.A2 and Dup.B2 between tRNA-I and tRNA-Q were repetitions of the Dup.A1 and the Dup.B1 formed by the tandem duplication and random loss. Panel A.c, Dup.A2 changed its direction by intramitochondrial recombination [35], forming the extant state. B, the recombination in Malcidae. Panel B.a, Dup.C1 was the original copy of thr repetition in the intergenic spacer between tRNA-H and ND4. Panel B.b, formation of the mini circle of Dup.C1 by intramitochondrial recombination [35]. Panel B.c, the mini circle of the Dup.C1 integrated into the control region of another mt-genome. Panel B.d, Dup.C2, the repetition of the Dup.C1, formed in the control region.

Mentions: In Alydidae, two subregions of the intergenic spacer between the tRNA-I and the tRNA-Q have a repeated counterpart (29 nt, with one site mutation, Blast E-value: 3e-9) and an exactly inverted repeated counterpart (26 nt, Blast E-value: 8e-10) in the control region (Figure 4A) (see Additional file 1). Since the TDRL model would only produce tandem duplications [34], these two repetitions are supposed to be formed by the TDRL following an intramitochondrial recombination [35] as shown in Figure 4A.


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

Hua J, Li M, Dong P, Cui Y, Xie Q, Bu W - BMC Genomics (2008)

Possible evolutionary mechanism of recombination in Alydidae and Malcidae. A, recombination in Alydidae. Panel A.a, the ancestral state. Dup.A1 and Dup.B1 were two original copies of the repetitions. Panel A.b, Dup.A2 and Dup.B2 between tRNA-I and tRNA-Q were repetitions of the Dup.A1 and the Dup.B1 formed by the tandem duplication and random loss. Panel A.c, Dup.A2 changed its direction by intramitochondrial recombination [35], forming the extant state. B, the recombination in Malcidae. Panel B.a, Dup.C1 was the original copy of thr repetition in the intergenic spacer between tRNA-H and ND4. Panel B.b, formation of the mini circle of Dup.C1 by intramitochondrial recombination [35]. Panel B.c, the mini circle of the Dup.C1 integrated into the control region of another mt-genome. Panel B.d, Dup.C2, the repetition of the Dup.C1, formed in the control region.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC2651891&req=5

Figure 4: Possible evolutionary mechanism of recombination in Alydidae and Malcidae. A, recombination in Alydidae. Panel A.a, the ancestral state. Dup.A1 and Dup.B1 were two original copies of the repetitions. Panel A.b, Dup.A2 and Dup.B2 between tRNA-I and tRNA-Q were repetitions of the Dup.A1 and the Dup.B1 formed by the tandem duplication and random loss. Panel A.c, Dup.A2 changed its direction by intramitochondrial recombination [35], forming the extant state. B, the recombination in Malcidae. Panel B.a, Dup.C1 was the original copy of thr repetition in the intergenic spacer between tRNA-H and ND4. Panel B.b, formation of the mini circle of Dup.C1 by intramitochondrial recombination [35]. Panel B.c, the mini circle of the Dup.C1 integrated into the control region of another mt-genome. Panel B.d, Dup.C2, the repetition of the Dup.C1, formed in the control region.
Mentions: In Alydidae, two subregions of the intergenic spacer between the tRNA-I and the tRNA-Q have a repeated counterpart (29 nt, with one site mutation, Blast E-value: 3e-9) and an exactly inverted repeated counterpart (26 nt, Blast E-value: 8e-10) in the control region (Figure 4A) (see Additional file 1). Since the TDRL model would only produce tandem duplications [34], these two repetitions are supposed to be formed by the TDRL following an intramitochondrial recombination [35] as shown in Figure 4A.

Bottom Line: Nucleotide sequences and the gene arrangements of mitochondrial genomes are effective tools for resolving phylogenetic problems.Two recombination events were found in Alydidae and Malcidae.Most sequences of the control regions did not appear to be important for regulatory functions.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology and Developmental Biology, Institute of Entomology, College of Life Sciences, Nankai University, Tianjin 300071, PR China. nkhuajimeng@163.com

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.

Show MeSH
Related in: MedlinePlus