Limits...
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.

Show MeSH

Related in: MedlinePlus

Possible evolutionary mechanism of the gene rearrangement in Largidae and Pyrrhocoridae. A, the putative ancestral arrangement; some regions of mtDNA including the tRNA-T and the tRNA-P were duplicated to form the intermediate (B) where some regions were lost to form C, Largidae D, Pyrrhocoridae. Dup.1-3 are the duplicated regions. The X in B indicates the randomly lost regions.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2651891&req=5

Figure 3: Possible evolutionary mechanism of the gene rearrangement in Largidae and Pyrrhocoridae. A, the putative ancestral arrangement; some regions of mtDNA including the tRNA-T and the tRNA-P were duplicated to form the intermediate (B) where some regions were lost to form C, Largidae D, Pyrrhocoridae. Dup.1-3 are the duplicated regions. The X in B indicates the randomly lost regions.

Mentions: The translocated tRNAs in Aradidae, Largidae, and Pyrrhocoridae have not changed their transcription direction. Although it is unknown what really happened to these mt-genomes causing the gene rearrangements and intergenic insertions, we tried to elucidate the possible evolutionary mechanisms using the most commonly supposed model for the gene rearrangements, including gene tandem duplication and random loss [4,31]. The possible mechanism of position switch of tRNA-T and tRNA-P in Largidae and Pyrrhocoridae is shown in Figure 3. The TDRL shown from Figure 3A (ancestral state) to Figure 3C (Largidae) and Figure 3D (Pyrrhocoridae) might include several different pathways. For example, the duplication of the Dup.2 is not necessary to produce Figure 3C and the Dup.3 is not necessary to Figure 3D, i.e., Largidae and Pyrrhocoridae might have been formed separately. However, because convergent rearrangements are rare in mt-genomes [33], and Largidae and Pyrrhocoridae are grouped as the monophyletic superfamily Pyrrhocoroidea (discussed later), these two rearrangements of tRNA-T and tRNA-P are speculated to be the products of the same intermediate and they are synapomorphies of the members of Pyrrhocoroidea. The translocation of the tRNA-Q in Aradidae could be elucidated with the same model.


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 the gene rearrangement in Largidae and Pyrrhocoridae. A, the putative ancestral arrangement; some regions of mtDNA including the tRNA-T and the tRNA-P were duplicated to form the intermediate (B) where some regions were lost to form C, Largidae D, Pyrrhocoridae. Dup.1-3 are the duplicated regions. The X in B indicates the randomly lost regions.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Possible evolutionary mechanism of the gene rearrangement in Largidae and Pyrrhocoridae. A, the putative ancestral arrangement; some regions of mtDNA including the tRNA-T and the tRNA-P were duplicated to form the intermediate (B) where some regions were lost to form C, Largidae D, Pyrrhocoridae. Dup.1-3 are the duplicated regions. The X in B indicates the randomly lost regions.
Mentions: The translocated tRNAs in Aradidae, Largidae, and Pyrrhocoridae have not changed their transcription direction. Although it is unknown what really happened to these mt-genomes causing the gene rearrangements and intergenic insertions, we tried to elucidate the possible evolutionary mechanisms using the most commonly supposed model for the gene rearrangements, including gene tandem duplication and random loss [4,31]. The possible mechanism of position switch of tRNA-T and tRNA-P in Largidae and Pyrrhocoridae is shown in Figure 3. The TDRL shown from Figure 3A (ancestral state) to Figure 3C (Largidae) and Figure 3D (Pyrrhocoridae) might include several different pathways. For example, the duplication of the Dup.2 is not necessary to produce Figure 3C and the Dup.3 is not necessary to Figure 3D, i.e., Largidae and Pyrrhocoridae might have been formed separately. However, because convergent rearrangements are rare in mt-genomes [33], and Largidae and Pyrrhocoridae are grouped as the monophyletic superfamily Pyrrhocoroidea (discussed later), these two rearrangements of tRNA-T and tRNA-P are speculated to be the products of the same intermediate and they are synapomorphies of the members of Pyrrhocoroidea. The translocation of the tRNA-Q in Aradidae could be elucidated with the same model.

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