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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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Schematic illustration of each event for mitochondrial gene rearrangement in C. fletcheri.Gene sizes are not drawn to scale. Gene names that are not underlined indicate a forward transcriptional direction, whereas underlines indicate a reverse transcriptional direction. tRNA genes are abbreviated using the one-letter amino acid code, with L*  =  trnL(UUR); S  =  trnS(AGN). White boxes represent genes with the same relative position as in the ancestral insect arrangement pattern. Yellow boxes represent gene translocations; red boxes represent gene inversions; green boxes represent gene shuffling with remote inversions compared to the ancestral insect arrangement. The grey boxes represent gene deletions. The remaining genes and gene orders identical to the ancestral insect are omitted. Each rearrangement event was independent, so there is no way of determining the order of event.
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pone-0042056-g006: Schematic illustration of each event for mitochondrial gene rearrangement in C. fletcheri.Gene sizes are not drawn to scale. Gene names that are not underlined indicate a forward transcriptional direction, whereas underlines indicate a reverse transcriptional direction. tRNA genes are abbreviated using the one-letter amino acid code, with L*  =  trnL(UUR); S  =  trnS(AGN). White boxes represent genes with the same relative position as in the ancestral insect arrangement pattern. Yellow boxes represent gene translocations; red boxes represent gene inversions; green boxes represent gene shuffling with remote inversions compared to the ancestral insect arrangement. The grey boxes represent gene deletions. The remaining genes and gene orders identical to the ancestral insect are omitted. Each rearrangement event was independent, so there is no way of determining the order of event.

Mentions: In contrast to the ancestral arrangement commonly found in insect mitochondrial genomes, C. fletcheri has a substantial number of tRNA rearrangements (Figure 6). These include 3 translocations resulting from 2 duplication/random deletion events (trnI, trnN, and trnR), 3 shuffling with remote inversions (trnQ, trnY, and trnC), and 1 local inversion (trnE). Several mechanisms responsible for mitochondrial gene rearrangement have been proposed: (1) translocation either by intramitochondrial recombination or by gene duplication/random loss, (2) inversion by intramitochondrial recombination, and (3) shuffling with remote inversion (translocation and inversion) either by combined intramitochondrial genome recombination and duplication/random loss of gene block, or by 2 separate intramitochondrial genome recombinations [47]–[51]. A schematic illustration of each possible event for C. fletcheri mitochondrial genome is presented in Figure 6. The translocation of trnI is probably caused by duplication of gene block trnI-trnQ-trnM-nad2, resulting in the arrangement trnI-trnQ-trnM-nad2-trnI-trnQ-trnM-nad2. A subsequent random loss of trnI in the first copy and trnQ-trnM-nad2 in the second copy may have resulted in trnQ-trnM-nad2-trnI. Likewise, the duplication/random loss of the gene blocks trnC-trnY and trnR-trnN may also have resulted in an intermediate arrangement of trnY-trnC and the current arrangement of trnN-trnR, respectively (Figure 6). The local inversion of trnE may have been caused by the breakage of the mitochondrial genome at trnE and recombination of the trnE on the other strand at the same position [48], [52]. In the case of the shuffling with remote inversion of 3 tRNAs (trnQ, trnY, and trnC), this may be caused by 2 separate intramitochondrial recombinations. The first inversion event may include recombination of trnQ and the gene block trnY-trnC in opposite directions, and the second translocation event may be caused by recombination of trnQ and trnY-trnC in the same directions, resulting in shuffling with remote inversion. Nevertheless, as each rearrangement event was independent, there is no way of determining the actual order of events.


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)

Schematic illustration of each event for mitochondrial gene rearrangement in C. fletcheri.Gene sizes are not drawn to scale. Gene names that are not underlined indicate a forward transcriptional direction, whereas underlines indicate a reverse transcriptional direction. tRNA genes are abbreviated using the one-letter amino acid code, with L*  =  trnL(UUR); S  =  trnS(AGN). White boxes represent genes with the same relative position as in the ancestral insect arrangement pattern. Yellow boxes represent gene translocations; red boxes represent gene inversions; green boxes represent gene shuffling with remote inversions compared to the ancestral insect arrangement. The grey boxes represent gene deletions. The remaining genes and gene orders identical to the ancestral insect are omitted. Each rearrangement event was independent, so there is no way of determining the order of event.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3412835&req=5

pone-0042056-g006: Schematic illustration of each event for mitochondrial gene rearrangement in C. fletcheri.Gene sizes are not drawn to scale. Gene names that are not underlined indicate a forward transcriptional direction, whereas underlines indicate a reverse transcriptional direction. tRNA genes are abbreviated using the one-letter amino acid code, with L*  =  trnL(UUR); S  =  trnS(AGN). White boxes represent genes with the same relative position as in the ancestral insect arrangement pattern. Yellow boxes represent gene translocations; red boxes represent gene inversions; green boxes represent gene shuffling with remote inversions compared to the ancestral insect arrangement. The grey boxes represent gene deletions. The remaining genes and gene orders identical to the ancestral insect are omitted. Each rearrangement event was independent, so there is no way of determining the order of event.
Mentions: In contrast to the ancestral arrangement commonly found in insect mitochondrial genomes, C. fletcheri has a substantial number of tRNA rearrangements (Figure 6). These include 3 translocations resulting from 2 duplication/random deletion events (trnI, trnN, and trnR), 3 shuffling with remote inversions (trnQ, trnY, and trnC), and 1 local inversion (trnE). Several mechanisms responsible for mitochondrial gene rearrangement have been proposed: (1) translocation either by intramitochondrial recombination or by gene duplication/random loss, (2) inversion by intramitochondrial recombination, and (3) shuffling with remote inversion (translocation and inversion) either by combined intramitochondrial genome recombination and duplication/random loss of gene block, or by 2 separate intramitochondrial genome recombinations [47]–[51]. A schematic illustration of each possible event for C. fletcheri mitochondrial genome is presented in Figure 6. The translocation of trnI is probably caused by duplication of gene block trnI-trnQ-trnM-nad2, resulting in the arrangement trnI-trnQ-trnM-nad2-trnI-trnQ-trnM-nad2. A subsequent random loss of trnI in the first copy and trnQ-trnM-nad2 in the second copy may have resulted in trnQ-trnM-nad2-trnI. Likewise, the duplication/random loss of the gene blocks trnC-trnY and trnR-trnN may also have resulted in an intermediate arrangement of trnY-trnC and the current arrangement of trnN-trnR, respectively (Figure 6). The local inversion of trnE may have been caused by the breakage of the mitochondrial genome at trnE and recombination of the trnE on the other strand at the same position [48], [52]. In the case of the shuffling with remote inversion of 3 tRNAs (trnQ, trnY, and trnC), this may be caused by 2 separate intramitochondrial recombinations. The first inversion event may include recombination of trnQ and the gene block trnY-trnC in opposite directions, and the second translocation event may be caused by recombination of trnQ and trnY-trnC in the same directions, resulting in shuffling with remote inversion. Nevertheless, as each rearrangement event was independent, there is no way of determining the actual order of events.

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