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Complete mitochondrial genome of the free-living earwig, Challia fletcheri (Dermaptera: Pygidicranidae) and phylogeny of Polyneoptera.

Wan X, Kim MI, Kim MJ, Kim I - PLoS ONE (2012)

Bottom Line: We sequenced the complete mitochondrial genome of the free-living earwig, Challia fletcheri, compared its genomic features to other available mitochondrial sequences from polyneopterous insects.The reversal pattern of skewness is explained in terms of inversion of replication origin.All phylogenetic analyses consistently placed Dermaptera as the sister to Plecoptera, leaving them as the most basal lineage of Polyneoptera or sister to Ephemeroptera, and placed Odonata consistently as the most basal lineage of the Pterygota.

View Article: PubMed Central - PubMed

Affiliation: College of Agriculture & Life Sciences, Chonnam National University, Gwangju, Republic of Korea.

ABSTRACT
The insect order Dermaptera, belonging to Polyneoptera, includes ∼2,000 extant species, but no dermapteran mitochondrial genome has been sequenced. We sequenced the complete mitochondrial genome of the free-living earwig, Challia fletcheri, compared its genomic features to other available mitochondrial sequences from polyneopterous insects. In addition, the Dermaptera, together with the other known polyneopteran mitochondrial genome sequences (protein coding, ribosomal RNA, and transfer RNA genes), were employed to understand the phylogeny of Polyneoptera, one of the least resolved insect phylogenies, with emphasis on the placement of Dermaptera. The complete mitochondrial genome of C. fletcheri presents the following several unusual features: the longest size in insects is 20,456 bp; it harbors the largest tandem repeat units (TRU) among insects; it displays T- and G-skewness on the major strand and A- and C-skewness on the minor strand, which is a reversal of the general pattern found in most insect mitochondrial genomes, and it possesses a unique gene arrangement characterized by a series of gene translocations and/or inversions. The reversal pattern of skewness is explained in terms of inversion of replication origin. All phylogenetic analyses consistently placed Dermaptera as the sister to Plecoptera, leaving them as the most basal lineage of Polyneoptera or sister to Ephemeroptera, and placed Odonata consistently as the most basal lineage of the Pterygota.

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Tandem repeat units (TRU) and secondary structures of trnL(UUR)-like and trnA-like sequences found in the TRU.(A) TRU; (B) The secondary structures of trnL(UUR)-like and trnA-like sequences found in the TRU. The sequences covered by yellow and green indicate each repeat unit; the underlined sequences indicate trnL(UUR)-like sequences; the italic nucleotides indicate trnA-like sequences; the rectangular boxes indicate the respective anticodons, and the nucleotide position is indicated at the beginning and end sites of the sequence.
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pone-0042056-g004: Tandem repeat units (TRU) and secondary structures of trnL(UUR)-like and trnA-like sequences found in the TRU.(A) TRU; (B) The secondary structures of trnL(UUR)-like and trnA-like sequences found in the TRU. The sequences covered by yellow and green indicate each repeat unit; the underlined sequences indicate trnL(UUR)-like sequences; the italic nucleotides indicate trnA-like sequences; the rectangular boxes indicate the respective anticodons, and the nucleotide position is indicated at the beginning and end sites of the sequence.

Mentions: Except for the A+T-rich region, a total of 24 non-coding regions ranging in size from 1 to 2,888 bp (a total of 3,784 bp) were interspersed throughout the C. fletcheri mitochondrial genome (Figure 1), and the total length is the longest in Polyneoptera (data not shown). Among these non-coding regions, the longest one (2,888 bp) is located between trnI and trnW, spanning a 2,876 bp tandem repeat unit (TRU) without coding any protein. This TRU consists of twenty-one 135-bp tandem repeats plus a 21-bp partial copy of the beginning of the repeat (Figure 4A). Within the TRU, 20 identical trnL(UUR)-like and 21 identical trnA-like sequences, along with the repeats, were identified by tRNA structure search. The sequence similarity between the regular and tRNA-like sequence was 51% for trnL(UUR) and 60% for trnA. These tRNA-like sequences fold into cloverleaf structures harboring the corresponding anticodons (Figure 4B), but their functionality remains unknown. The 75.60% A/T content in the TRU is higher than that of the whole genome (13 PCGs, rrnL, and rrnS), but lower than that of the A+T-rich region (Table S1). To our knowledge, the size of this TRU is the longest reported in insects to date. In Hemiptera, a 1,513-bp long TRU located between trnE and trnF was found in the A. pisum mitochondrial genome (Unpublished, GenBank: FJ411411). This TRU contains seven 202-bp tandem repeats with the first repeat unit overlapping with the 3′ end of trnE, and a partial 99-bp copy of the beginning of the repeat. Similarly, a 1,724-bp long TRU has also been reported from the coleopteran, Pyrocoelia rufa[8]. In addition, a 409-bp long TRU including 4 identical trnL(UUR), which all were presumed to be functional was reported in the hymenopteran Abispa ephippium[38]. However, a similar TRU has never been found in the other mitochondrial genomes of Polyneoptera. Such TRUs in animal mitochondrial genomes could originate from slipped-strand mispairing, resulting in expanded repeat caused by an unequal crossing-over event due to the mispairing propensity of the simple tandem repeats [39].


Complete mitochondrial genome of the free-living earwig, Challia fletcheri (Dermaptera: Pygidicranidae) and phylogeny of Polyneoptera.

Wan X, Kim MI, Kim MJ, Kim I - PLoS ONE (2012)

Tandem repeat units (TRU) and secondary structures of trnL(UUR)-like and trnA-like sequences found in the TRU.(A) TRU; (B) The secondary structures of trnL(UUR)-like and trnA-like sequences found in the TRU. The sequences covered by yellow and green indicate each repeat unit; the underlined sequences indicate trnL(UUR)-like sequences; the italic nucleotides indicate trnA-like sequences; the rectangular boxes indicate the respective anticodons, and the nucleotide position is indicated at the beginning and end sites of the sequence.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3412835&req=5

pone-0042056-g004: Tandem repeat units (TRU) and secondary structures of trnL(UUR)-like and trnA-like sequences found in the TRU.(A) TRU; (B) The secondary structures of trnL(UUR)-like and trnA-like sequences found in the TRU. The sequences covered by yellow and green indicate each repeat unit; the underlined sequences indicate trnL(UUR)-like sequences; the italic nucleotides indicate trnA-like sequences; the rectangular boxes indicate the respective anticodons, and the nucleotide position is indicated at the beginning and end sites of the sequence.
Mentions: Except for the A+T-rich region, a total of 24 non-coding regions ranging in size from 1 to 2,888 bp (a total of 3,784 bp) were interspersed throughout the C. fletcheri mitochondrial genome (Figure 1), and the total length is the longest in Polyneoptera (data not shown). Among these non-coding regions, the longest one (2,888 bp) is located between trnI and trnW, spanning a 2,876 bp tandem repeat unit (TRU) without coding any protein. This TRU consists of twenty-one 135-bp tandem repeats plus a 21-bp partial copy of the beginning of the repeat (Figure 4A). Within the TRU, 20 identical trnL(UUR)-like and 21 identical trnA-like sequences, along with the repeats, were identified by tRNA structure search. The sequence similarity between the regular and tRNA-like sequence was 51% for trnL(UUR) and 60% for trnA. These tRNA-like sequences fold into cloverleaf structures harboring the corresponding anticodons (Figure 4B), but their functionality remains unknown. The 75.60% A/T content in the TRU is higher than that of the whole genome (13 PCGs, rrnL, and rrnS), but lower than that of the A+T-rich region (Table S1). To our knowledge, the size of this TRU is the longest reported in insects to date. In Hemiptera, a 1,513-bp long TRU located between trnE and trnF was found in the A. pisum mitochondrial genome (Unpublished, GenBank: FJ411411). This TRU contains seven 202-bp tandem repeats with the first repeat unit overlapping with the 3′ end of trnE, and a partial 99-bp copy of the beginning of the repeat. Similarly, a 1,724-bp long TRU has also been reported from the coleopteran, Pyrocoelia rufa[8]. In addition, a 409-bp long TRU including 4 identical trnL(UUR), which all were presumed to be functional was reported in the hymenopteran Abispa ephippium[38]. However, a similar TRU has never been found in the other mitochondrial genomes of Polyneoptera. Such TRUs in animal mitochondrial genomes could originate from slipped-strand mispairing, resulting in expanded repeat caused by an unequal crossing-over event due to the mispairing propensity of the simple tandem repeats [39].

Bottom Line: We sequenced the complete mitochondrial genome of the free-living earwig, Challia fletcheri, compared its genomic features to other available mitochondrial sequences from polyneopterous insects.The reversal pattern of skewness is explained in terms of inversion of replication origin.All phylogenetic analyses consistently placed Dermaptera as the sister to Plecoptera, leaving them as the most basal lineage of Polyneoptera or sister to Ephemeroptera, and placed Odonata consistently as the most basal lineage of the Pterygota.

View Article: PubMed Central - PubMed

Affiliation: College of Agriculture & Life Sciences, Chonnam National University, Gwangju, Republic of Korea.

ABSTRACT
The insect order Dermaptera, belonging to Polyneoptera, includes ∼2,000 extant species, but no dermapteran mitochondrial genome has been sequenced. We sequenced the complete mitochondrial genome of the free-living earwig, Challia fletcheri, compared its genomic features to other available mitochondrial sequences from polyneopterous insects. In addition, the Dermaptera, together with the other known polyneopteran mitochondrial genome sequences (protein coding, ribosomal RNA, and transfer RNA genes), were employed to understand the phylogeny of Polyneoptera, one of the least resolved insect phylogenies, with emphasis on the placement of Dermaptera. The complete mitochondrial genome of C. fletcheri presents the following several unusual features: the longest size in insects is 20,456 bp; it harbors the largest tandem repeat units (TRU) among insects; it displays T- and G-skewness on the major strand and A- and C-skewness on the minor strand, which is a reversal of the general pattern found in most insect mitochondrial genomes, and it possesses a unique gene arrangement characterized by a series of gene translocations and/or inversions. The reversal pattern of skewness is explained in terms of inversion of replication origin. All phylogenetic analyses consistently placed Dermaptera as the sister to Plecoptera, leaving them as the most basal lineage of Polyneoptera or sister to Ephemeroptera, and placed Odonata consistently as the most basal lineage of the Pterygota.

Show MeSH
Related in: MedlinePlus