Mitochondrial genomes of two Sinochloraspecies (Orthoptera): novel genome rearrangements and recognition sequence of replication origin
© Liu et al.; licensee BioMed Central Ltd. 2013
Received: 23 September 2012
Accepted: 31 January 2013
Published: 20 February 2013
Orthoptera, the largest polyneopteran insect order, contains 2 suborders and 235 subfamilies. Orthoptera mitochondrial genomes (mitogenomes) follow the ancestral insect gene order, with the exception of a trnD-trnK rearrangement in Acridomorphs and rare tRNA inversions. A question still remains regarding whether a long thymine-nucleotide stretch (T-stretch) involved in the recognition of the replication origin exists in the control region (CR) of Orthoptera mitochondrial DNA (mtDNA). Herein, we completed the sequencing of whole mitogenomes of two congeners (Sinochlora longifissa and S. retrolateralis), which possess overlapping distribution areas. Additionally, we performed comparative mitogenomic analysis to depict evolutionary trends of Orthoptera mitogenomes.
Both Sinochlora mitogenomes possess 37 genes and one CR, a common gene orientation, normal structures of transfer RNA and ribosomal RNA genes, rather low A+T bias, and significant C skew in the majority strand (J-strand), resembling all the other sequenced ensiferans. Both mitogenomes are characterized by (1) a large size resulting from multiple copies of an approximately 175 bp GC-rich tandem repeat within CR; (2) a novel gene order (rrnS-trnI-trnM-nad2-CR-trnQ-trnW), compared to the ancestral order (rrnS-CR-trnI-trnQ-trnM-nad2-trnW); and (3) redundant trnS(UCN) pseudogenes located between trnS(UCN) and nad1. Multiple independent duplication events followed by random and/or non-random loss occurred during Sinochlora mtDNA evolution. The Orthoptera mtDNA recognition sequence of the replication origin may be one of two kinds: a long T-stretch situated in or adjacent to a possible stem-loop structure or a variant of a long T-stretch located within a potential stem-loop structure.
The unique Sinochlora mitogenomes reveal that the mtDNA architecture within Orthoptera is more variable than previously thought, enriching our knowledge on mitogenomic genetic diversities. The novel genome rearrangements shed light on mtDNA evolutionary patterns. The two kinds of recognition sequences of replication origin suggest that the regulatory sequences involved in the replication initiation process of mtDNA have diverged through Orthoptera evolution.
KeywordsSinochlora longifissa Sinochlora retrolateralis Mitochondrial genome Genome rearrangements Recognition sequence
Insect mitogenomes are generally compact with few intergenic spacers and possess stable gene content and organization. They are usually about 16 kb in size and bear 13 protein-coding genes (PCGs), 2 ribosomal RNA genes (rRNAs), 22 transfer RNA genes (tRNAs), and one control region (CR) that includes replication and transcription origins . However, extensive studies have revealed that gene order rearrangement and size variation that results from the presence of tandem repeats (TRs) and other non-coding regions occur more often than previously expected. Much attention has been paid to studies focusing on unveiling genomic diversities and evolutionary trends. Recently, a mitogenomic investigation of congeneric species has yielded a valuable approach for assessing mtDNA evolutionary trends . Unfortunately, in spite of the large number of insect species, the limited availability of complete mitogenomic sequence data, including those of congeneric species, impedes a thorough understanding of the insect mitogenomes.
Orthoptera, the largest polyneopteran order, contains 235 subfamilies and over 22,500 described species, taxonomically divided into two suborders: Caelifera (locusts and grasshoppers) and Ensifera (katydids and crickets etc.) . Orthoptera mitogenomes generally possess a relatively stable gene content and organization identical to the insect ancestor . Only a trnD-trnK rearrangement in the lineage Acridomorpha [4, 5], inversion of the gene cluster trnE-trnS(AGN)-trnN in Teleogryllus emma, and occasional inversion of trnW in the migratory locust  have been discovered. A mitogenomic divergence in the AT-bias between the two suborders has been demonstrated, i.e., the AT-content was generally lower in Ensifera than in Caelifera . Additionally, a possible stem-loop structure has been implicated in mtDNA replication initiation in a few caeliferans [8, 9], which contrasts with the recognition of the mtDNA replication origin (OR) that involves a long T-stretch in most other insects . However, representative katydid mitogenomes, e.g., Anabrus simplex and Deracantha onos, revealed the existence of a long T-stretch [10, 11]. Furthermore, mitogenomes of 27 Caelifera and 10 Ensifera species available from GenBank demonstrate a distinct taxon sampling imbalance between the two suborders. Thus, additional Ensifera taxon sampling is essential to investigate the mitogenomic genetic diversities and evolutionary trends.
The genus Sinochlora Tinkham , Chinese bush katydid, belongs to the subfamily Phaneropterinae in the suborder Ensifera. In Sinochlora, one species S. longifissa is widespread in East Asia including Japan, Korea, and southern China, and two species are widely distributed and indigenous in southern China . Other species are endemic in various large mountains in southern China including low-altitude areas in Tibet [13, 14]. Investigation of the mitogenomic evolutionary trends of the genus is helpful to unveil the molecular mechanism of the divergence patterns.
Herein, we chose two representative species, S. longifissa distributed in East Asia, and S. retrolateralis narrowly endemic in southern China, for mitogenomic investigation. We sequenced the mitogenomes of the two congeners, unveiled novel mitogenomic characteristics, and outlined the possible rearrangement mechanism. Additionally, we also compared the recognition sequences of the OR in known Orthoptera mitogenomes. Overall, we attempted to provide the molecular basis for understanding diversification of the genus Sinochlora and depict molecular diversity and evolutionary trends of Orthoptera mitogenomes.
Results and discussion
Mitogenome organization of the two Sinochlora species
Start and stop codons
All PCGs except cox1 and nad6 start with typical ATN codons. A previous study concerning Orthoptera mitogenomes suggested that the cox1 gene may start with an irregular tetranucleotide codon AUGA . Similar irregular tetranucleotide codons were also proposed as start codons in Drosophila[18, 19]. However, there is no experimental evidence for the use of a 4-bp start codon in any creature. Recent research on characteristics of mature mRNA and rRNA genes from D. melanogaster mitochondria showed that UCG serves as the start codon of its cox1 gene . The result is consistent with predictions of the start of cox1 suggested by comparison of conserved amino acid positions . By comparing amino acid sequences of cox1 in all sequenced Orthoptera, we observed that the first conserved codon is the TCN serine codon, downstream of which at least three codon positions are also conserved and there are no standard ATN bases (Additional file 2). Thus, in both Sinochlora species, the conserved TCT serine codon may also serve as a start codon. Concerning the nad6 gene, it has been proposed to start with ATN codons in other sequenced orthopterans; however, there are no conserved amino acid positions within the span of over 50 amino acids downstream of trnP (Additional file 3). Then we propose that the nad6 may start with CTG in S. longifissa and TTG in S. retrolateralis, considering previous designation of such start codons [22, 23]. The two start codons, creating no IGS or overlap between trnP and nad6 genes, also appear to be more plausible in the evolutionary economic perspective .
Two standard stop codons TAA/TAG and two incomplete stop codons T/TA are utilized in the PCGs. For S. longifissa, six PCGs (nad2, atp8, atp6, cox3, nad3, and nad4L) terminate with TAA, one (nad1) with TAG, one (nad6) with TA, and the other four (cox1, nad5, nad4, and cob) with T. The stop codons differ between the two congeners in that TAA is utilized as the cox2 stop codon, and TA is utilized as the atp6 and cox3 stop codon in S. retrolateralis. A partial T or TA stop codon, which was proposed to create complete TAA stop codons via posttranscriptional polyadenylation , is also present in other metazoan mitochondrial genes.
Novel gene order rearrangement involving the control region
One of our most significant findings is the novel gene order rearrangement "rrnS-trnI-trnM-nad2-CR-trnQ-trnW" in both Sinochlora species (Figure 1). The two mitogenomes are the first representatives that have a large-scale translocation involving the CR in Orthoptera. Such gene order has not been observed in other sequenced insect mitogenomes. The gene cluster rrnS-CR-trnI-trnQ-trnM-nad2 in the proposed ancestral mitogenome has been discovered to function as a hot spot for gene rearrangements in arthropod mitogenomes. Duplicate trnI and partial trnQ genes have been discovered in the CR close to the rrnS gene in some blowflies [25, 26]. In a mantid, a complicate set of repeat units dispersing in both ends of the CR also translocated between trnM and nad2. A plague thrips displayed CR duplications that are distant from the rRNA genes . Various locations of the CR and neighboring tRNA genes have been exhibited in lice . Location variability of the putative CR has also been reported as a product of the tRNA gene translocation, such as rrnS-trnQ-CR-trnI-trnS(UCN)-trnM-nad2 in a springtail , or the tRNA and rRNA gene translocation, such as rrnL-trnV-trnS(UCN)-trnC-CR-rrnS in a mite . The CR and the neighboring genes have also been found to be duplicated in some ticks .
Organization of the control region
In S. longifissa, the TR region is 1,731 bp in length, comprising nine full 175-bp copies and a partial 153-bp copy. In S. retrolateralis, a total of five 175-bp repeat copies have been successfully sequenced from both ends of the TR; however, we failed to sequence through the whole TR region due to the presence of a large number of repeat copies. We estimate that there are twelve 175-bp tandem copies in S. retrolateralis based on the length (~2,100 bp) of the TR indicated by gel electrophoresis. The consensus TR motifs of the two species share 61.2% sequence identity. In S. longifissa, four of the nine TR motifs are identical to the consensus TR motif, and the other five have a few mutations and/or deletions. Among the nine TR motifs, all but the fourth possess an ORF. The consensus ORF could be translated into 58 amino acids, starting with lysine (AAA) and ending with valine (GTG) (Additional file 4). Low shared identities (< 45%) with nuclear sequences in search of the GenBank database exclude the possibility that the ORF is transferred from the nuclear genome. It has 47.1% identity with the antisense strand of nad4, and 45.9% identity with the sense strand of cox1. The shared bases are scattered in alignment, among which over 60% are A and T (Additional file 5). This suggests that the ORF might not be obtained through horizontal transfer between mitochondria. In contrast, no ORF could be found in the S. retrolateralis TR motif.
The TR motif could be duplicated through slipped-strand mispairing [34, 35]. Moreover, potential stem-loop structures in a repeated unit and its flanking part have been demonstrated to cause an increase in slipped-strand mispairing frequency [35, 36]. Stem-loop structures were detected in the TR region of the two Sinochlora species. For example, in the first TR unit and its junctions at both ends in S. longifissa, the nucleotide sequence can potentially form seven 8- to 27-bp hairpins with 5- to 10-bp loops supported by 1–5 GC matches in the stem (Figure 3C). In the corresponding regions in S. retrolateralis, the nucleotide sequence can potentially form six 10- to 29-bp hairpins with 5- to 15-bp loops supported by 1–4 GC matches in the stem (Figure 3D). Similar complicated hairpin structures in TR were also detected in the louse Bothriometopus and termites [37, 38]. However, there are no conserved stem-loops among the TRs and at the joints in these insects.
Unassigned intergenic spacers and trnS(UCN)pseudogenes
Eleven IGSs with identical locations are present in S. longifissa (totalling 318 bp) and S. retrolateralis (263 bp); one additional IGS is situated between atp6 and cox3 in S. longfissa (2 bp) and between cox2 and trnK in S. retrolateralis (1 bp) (Table 1). The largest IGS (161 bp for S. longifissa and 94 bp for S. retrolateralis) lies between trnS(UCN) and nad1. By comparing the IGS of currently available Orthoptera mitogenomes, we found a 7-bp conserved motif (THYTHDA) downstream the nad1 across Orthoptera, with the only exception of Mekongiella xizangensis (Additional file 6). The conserved motif has been proposed as a binding site for mitochondrial transcription termination factor (mtTERM) in Orthoptera . Similar conserved motifs, which were proposed as a binding site of the mtTERM, between trnS(UCN) and nad1 have also been found in Lepidoptera , and Coleoptera . It has been confirmed that one of the two binding sites of mtTERM lies downstream of nad1 in Drosophila[41, 42].
Relative-Rate Test results for contrasts between trnS(UCN) genes and pseudogenes
All S. Ser versus all S. pSer
0.338989 versus 0.675022
Sr-Ser vesus Sr-pSer
0.364826 versus 0.791345
Sl-Ser vesus Sl-pSer
0.297057 versus 0.604668
Mechanism of genome rearrangements
Recognition sequences of replication origins
Human mtDNA synthesis is initiated from the sites near the stem base of the secondary structure located around the light strand origin, and the small T-stretch (6–11 bp) located in the loop portion participates in the initiation process . The secondary structure in human and other vertebrate mtDNA is very similar to the aforementioned stem-loop structure in the orthopterans . Therefore, the long T-stretch, which participates in the formation of or is adjacent to a possible stem-loop structure in katydids, and the T-stretch variants within the stem-loop structure of crickets and most grasshoppers, could also play a crucial role in mtDNA replication initiation. Notably, the T-stretch in cockroaches and termites also participates in the formation of a certain stem-loop structure (Additional file 8). However, the stem-loop structure around the mtDNA OR could not be detected in Drosophila. Therefore, the OR recognition sequences of mtDNA, although generally detected in Orthoptera, have diverged not only among Orthoptera but also throughout insect evolution.
The two Sinochlora congeners represent the first two orthopterans that have a large-scale translocation involving the CR. It seems that the present mitogenome rearrangements are a consequence of tandem duplication followed by non-random loss of paralogs. However, future research including additional taxon sampling is needed to determine rearrangement mechanisms and evolutionary processes. Comparison of the OR recognition sequences among Orthoptera and other insects will aid in further understanding of mechanisms underlying mtDNA replication. Divergence in nucleotide bias and skew of mtDNA exists between the two suborders of Orthoptera. Future studies on mtDNA-based phylogeny of Orthoptera should therefore take into consideration the base compositional heterogeneity, which could lead to incorrect phylogenetic inferences [47, 48].
Taxon sampling and mitochondria DNA extraction
Specimens of S. longifissa and S. retrolateralis were collected from Wuyi Mountain, Fujian, South China in 2005. The specimens were preserved in 95% ethanol and stored at 4°C. The mitochondria were isolated as previously described , and mtDNA was extracted with the DNeasy Blood & Tissue Kit (Qiagen).
First, short gene regions within individual genes (cox1, cox3, cytb, nad1, rrnL, and rrnS) were amplified and sequenced using listed primers (Additional file 9). Then the obtained sequences were used to design specific primers for amplifying overlapping fragments spanning the whole mitogenomes.
Fragments larger than 3 kb were amplified using TaKaRa LA Taq™ (Takara, Dalian, China), with the following cycling conditions: an initial denaturation at 94°C for 3 min, followed by 36 cycles of denaturation at 94°C for 30 s, annealing at 50–57°C for 30 s, and extension at 68°C for 3–8 min (1 kb/min), with a final elongation at 68°C for 6 min after the last cycle. 16 fragments smaller than 3 kb were performed using TaKaRa ExTaq™ or TaKaRa rTaq™ (Takara, Dalian, China), with the following cycling conditions: an initial denaturation at 94°C for 3 min, followed by 36 cycles of denaturation at 94°C for 30 s, annealing at 45–60°C for 30 s, and extension at 72°C for 1–2 min (1 kb/min), with a final elongation at 72°C for 6 min after the last cycle. After purification with AxyPrep™ DNA Gel Extraction Kit, most PCR products were directly sequenced by means of primer walking, and other fragments were cloned into the pGEM-T Easy vector (Promega, USA) prior to sequencing.
Concerning the CR, long PCR amplicons were successfully amplified, which encompassed the entire CR from nad1 to cox2 genes for both species, but gel electrophoresis showed multiple bands. The largest and brightest band was chosen to clone into the pGEM-T Easy vector for sequencing. Sequencing primers were designed from flanking regions of the whole TR region and subsequently a 400-bp sequence at each end was obtained. The obtained TR units were analyzed with the TRF4.0 software  in order to design suitable primers for walking. For S. longifissa, the complete TR region was sequenced using specific primers that was designed based on a mutant poly C (8 continuous C) (Additional file 4) in one of the TR units. For S. retrolateralis, the length of the PCR product indicates that the TR region is about 2,100 bp, suggesting that there are 12 complete tandem repeats; however, only 5 of these tandem repeats were sequenced.
Sequence assembly, annotation and secondary structure prediction
The complete mitogenome sequences were assembled using the SeqMan program from the Lasergene package software (DNAStar, Madison, WI). tRNA genes were identified by their cloverleaf secondary structures using tRNAscan-SE 1.21 . The locations of 13 PCGs and rRNA genes were determined by comparison of homologous sequences with other sequenced orthopterans using the CLUSTAL W programs . Nucleotide composition statistics, nucleotide bias and skew of the orthopterans (Additional file 10) except those at P4fd, were retrieved from the METAMiGA database . Skewness was calculated to describe strand bias , which measures the relative number of As to Ts (AT skew = [A - T]/[A + T]) and Gs to Cs (GC skew = [G - C]/[G + C]). We obtained codon usage from the SMS2 website  and computed AT and GC skew at the P4fd on the J-strand. Potential stem-loop structures of the polyneopterans (Additional file 10) were predicted by the Mfold software . Repeat sequences were identified with the TRF4.0 software. ORF was detected using the MEGA5 software .
Divergence and substitution rates between trnS(UCN) genes and pseudogenes were investigated, using trnS(UCN) of Myrmecophilus manni as outgroup. Gapped positions were eliminated from the resulted alignment. The remaining 44 sites (including 26 parsimony informative) were used to reconstruct a distance phylogeny by Minimum Evolution using JC distances , due to the low number of sites analyzed. Relative-rate tests  were used to calculate substitution rates employing RRTree version 1.1.11 , presuming JC distances.
- atp6 and atp8:
ATP synthase subunits 6 and 8
Cytochrome c oxidase subunits 1 to 3
- nad1–6 and nad4L:
NADH dehydrogenase subunits 1 to 6 and 4L
- rrnS and rrnL:
Small and large ribosomal RNA (rRNA) subunits
Transfer RNA genes where X is the one-letter abbreviation of the corresponding amino acid
We thank Dr. Le Kang (CAS) for his valuable direction and assistance in the project design, coordination and implementation, as well as critical revision of the original manuscript. We also thank two anonymous reviewers for their valuable comments. This study is supported by the grants from the Natural Science Foundation of China (No. 31071953).
- Boore JL: Animal mitochondrial genomes. Nucleic Acids Res. 1999, 27: 1767-1780. 10.1093/nar/27.8.1767.PubMed CentralView ArticlePubMedGoogle Scholar
- Gissi C, Iannelli F, Pesole G: Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. Heredity. 2008, 101: 301-320. 10.1038/hdy.2008.62.View ArticlePubMedGoogle Scholar
- Eades D, Otte D, Cigliano M, Braun H: Orthoptera Species File Online. 2013, Version 2.0/4.1. http://Orthoptera.SpeciesFile.orgGoogle Scholar
- Sheffield NC, Hiatt KD, Valentine MC, Song H, Whiting MF: Mitochondrial genomics in Orthoptera using MOSAS. Mitochondr DNA. 2010, 21: 87-104. 10.3109/19401736.2010.500812.View ArticleGoogle Scholar
- Flook P, Rowell H, Gellissen G: Homoplastic rearrangements of insect mitochondrial tRNA genes. Naturwissenschaften. 1995, 82: 336-337. 10.1007/BF01131531.View ArticleGoogle Scholar
- Ye W, Dang JP, Xie LD, Huang Y: Complete mitochondrial genome of Teleogryllus emma (Orthoptera: Gryllidae) with a new gene order in Orthoptera. Zool Res. 2008, 29: 236-244. 10.3724/SP.J.1141.2008.00236.View ArticleGoogle Scholar
- Ma C, Yang P, Jiang F, Chapuis MP, Shali Y, Sword GA, Kang L: Mitochondrial genomes reveal the global phylogeography and dispersal routes of the migratory locust. Mol Ecol. 2012, 21: 4344-4358. 10.1111/j.1365-294X.2012.05684.x.View ArticlePubMedGoogle Scholar
- Saito S, Tamura K, Aotsuka T: Replication origin of mitochondrial DNA in insects. Genetics. 2005, 171: 1695-1705. 10.1534/genetics.105.046243.PubMed CentralView ArticlePubMedGoogle Scholar
- Zhang DX, Hewitt GM: Insect mitochondrial control region: A review of its structure, evolution and usefulness in evolutionary studies. Biochem Syst Ecol. 1997, 25: 99-120. 10.1016/S0305-1978(96)00042-7.View ArticleGoogle Scholar
- Zhou Z, Huang Y, Shi F, Ye H: The complete mitochondrial genome of Deracantha onos (Orthoptera: Bradyporidae). Mol Biol Rep. 2009, 36: 7-12. 10.1007/s11033-007-9145-8.View ArticlePubMedGoogle Scholar
- Fenn JD, Cameron SL, Whiting MF: The complete mitochondrial genome sequence of the Mormon cricket (Anabrus simplex: Tettigoniidae: Orthoptera) and an analysis of control region variability. Insect Mol Biol. 2007, 16: 239-252. 10.1111/j.1365-2583.2006.00721.x.View ArticlePubMedGoogle Scholar
- Tinkham ER: Sinochlora, a new Tettigoniid genus from China with description of five new species (Orthoptera). Trans Amer Entomol Soc. 1945, 70: 235-246.Google Scholar
- Liu CX, Kang L: Revision of the genus Sinochlora Tinkham (Orthoptera: Tettigoniidae, Phaneropterinae). J Nat Hist. 2007, 41: 1313-1341. 10.1080/00222930701437667.View ArticleGoogle Scholar
- Wang G, Lu RS, Shi FM: Remarks on the genus Sinochlora Tinkham (Orthoptera: Tettigoniidae, Phaneropterinae). Zootaxa. 2012, 3526: 1-16.Google Scholar
- Kimura M: The neutral theory of molecular evolution. 1983, Cambridge: Cambridge University PressView ArticleGoogle Scholar
- Bulmer M: The selection-mutation-drift theory of synonymous codon usage. Genetics. 1991, 129: 897-907.PubMed CentralPubMedGoogle Scholar
- Hassanin A, Leger N, Deutsch J: Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of Metazoa, and consequences for phylogenetic inferences. Syst Biol. 2005, 54: 277-298. 10.1080/10635150590947843.View ArticlePubMedGoogle Scholar
- Clary DO, Wolstenholme DR: The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985, 22: 252-271. 10.1007/BF02099755.View ArticlePubMedGoogle Scholar
- Satta Y, Ishiwa H, Chigusa SI: Analysis of nucleotide substitutions of mitochondrial DNAs in Drosophila melanogaster and its sibling species. Mol Biol Evol. 1987, 4: 638-650.PubMedGoogle Scholar
- Stewart JB, Beckenbach AT: Characterization of mature mitochondrial transcripts in Drosophila, and the implications for the tRNA punctuation model in arthropods. Gene. 2009, 445: 49-57. 10.1016/j.gene.2009.06.006.View ArticlePubMedGoogle Scholar
- Beard CB, Mills Hamm D, Collins FH: The mitochondrial genome of the mosquito Anopheles gambiae: DNA sequence, genome organization, and comparisons with mitochondrial sequences of other insects. Insect Mol Biol. 1993, 2: 103-124. 10.1111/j.1365-2583.1993.tb00131.x.View ArticlePubMedGoogle Scholar
- Bae JS, Kim I, Sohn HD, Jin BR: The mitochondrial genome of the firefly, Pyrocoelia rufa: complete DNA sequence, genome organization, and phylogenetic analysis with other insects. Mol Phylogenet Evol. 2004, 32: 978-985. 10.1016/j.ympev.2004.03.009.View ArticlePubMedGoogle Scholar
- Cameron SL, Johnson KP, Whiting MF: The mitochondrial genome of the screamer louse Bothriometopus (Phthiraptera: Ischnocera): Effects of extensive gene rearrangements on the evolution of the genome. J Mol Evol. 2007, 65: 589-604. 10.1007/s00239-007-9042-8.View ArticlePubMedGoogle Scholar
- Ojala D, Montoya J, Attardi G: tRNA punctuation model of RNA processing in human mitochondria. Nature. 1981, 290: 470-474. 10.1038/290470a0.View ArticlePubMedGoogle Scholar
- Lessinger AC, Junqueira ACM, Conte FF, Espin A: Analysis of a conserved duplicated tRNA gene in the mitochondrial genome of blowflies. Gene. 2004, 339: 1-6.View ArticlePubMedGoogle Scholar
- Nelson LA, Lambkin CL, Batterham P, Wallman JF, Dowton M, Whiting MF, Yeates DK, Cameron SL: Beyond barcoding: A mitochondrial genomics approach to molecular phylogenetics and diagnostics of blowflies (Diptera: Calliphoridae). Gene. 2012, 511: 131-142. 10.1016/j.gene.2012.09.103.View ArticlePubMedGoogle Scholar
- Cameron SL, Barker SC, Whiting MF: Mitochondrial genomics and the new insect order Mantophasmatodea. Mol Phylogenet Evol. 2006, 38: 274-279. 10.1016/j.ympev.2005.09.020.View ArticlePubMedGoogle Scholar
- Shao RF, Barker SC: The highly rearranged mitochondrial genome of the plague thrips, Thrips imaginis (Insecta: thysanoptera): Convergence of two novel gene boundaries and an extraordinary arrangement of rRNA genes. Mol Biol Evol. 2003, 20: 362-370. 10.1093/molbev/msg045.View ArticlePubMedGoogle Scholar
- Cameron SL, Yoshizawa K, Mizukoshi A, Whiting MF, Johnson KP: Mitochondrial genome deletions and minicircles are common in lice (Insecta: Phthiraptera). BMC Genomics. 2011, 12: 394-10.1186/1471-2164-12-394.PubMed CentralView ArticlePubMedGoogle Scholar
- Nardi F, Carapelli A, Fanciulli PP, Dallai R, Frati F: The complete mitochondrial DNA sequence of the basal Hexapod Tetrodontophora bielanensis: Evidence for heteroplasmy and tRNA translocations. Mol Biol Evol. 2001, 18: 1293-1304. 10.1093/oxfordjournals.molbev.a003914.View ArticlePubMedGoogle Scholar
- Navajas M, Le Conte Y, Solignac M, Cros-Arteil S, Cornuet JM: The complete sequence of the mitochondrial genome of the honeybee ectoparasite mite Varroa destructor (Acari: Mesostigmata). Mol Biol Evol. 2002, 19: 2313-2317. 10.1093/oxfordjournals.molbev.a004055.View ArticlePubMedGoogle Scholar
- Shao RF, Barker SC, Mitani H, Aoki Y, Fukunaga M: Evolution of duplicate control regions in the mitochondrial genomes of Metazoa: A case study with Australasian Ixodes ticks. Mol Biol Evol. 2005, 22: 620-629.View ArticlePubMedGoogle Scholar
- Fenn JD, Song H, Cameron SL, Whiting MF: A preliminary mitochondrial genome phylogeny of Orthoptera (Insecta) and approaches to maximizing phylogenetic signal found within mitochondrial genome data. Mol Phylogenet Evol. 2008, 49: 59-68. 10.1016/j.ympev.2008.07.004.View ArticlePubMedGoogle Scholar
- Boore JL: The duplication/random loss model for gene rearrangement exemplified by mitochondrial genomes of deuterostome animals. Comparative genomics, computational biology series. Edited by: Sankoff D, Nadeau J. 2000, Netherlands: Dordrecht, 133-147. 1Google Scholar
- Levinson G, Gutman GA: Slipped-strand mispairing: A major mechanism for DNA sequence evolution. Mol Biol Evol. 1987, 4: 203-221.PubMedGoogle Scholar
- Broughton RE, Dowling TE: Length variation in mitochondrial DNA of the minnow Cyprinella spiloptera. Genetics. 1994, 138: 179-190.PubMed CentralPubMedGoogle Scholar
- Cameron SL, Lo N, Bourguignon T, Svenson GJ, Evans TA: A mitochondrial genome phylogeny of termites (Blattodea: Termitoidae): Robust support for interfamilial relationships and molecular synapomorphies define major clades. Mol Phylogenet Evol. 2012, 65: 163-173. 10.1016/j.ympev.2012.05.034.View ArticlePubMedGoogle Scholar
- Cameron SL, Whiting MF: Mitochondrial genomic comparisons of the subterranean termites from the Genus Reticulitermes (Insecta: Isoptera: Rhinotermitidae). Genome. 2007, 50: 188-202. 10.1139/g06-148.View ArticlePubMedGoogle Scholar
- Cameron SL, Whiting MF: The complete mitochondrial genome of the tobacco hornworm, Manduca sexta, (Insecta: Lepidoptera: Sphingidae), and an examination of mitochondrial gene variability within butterflies and moths. Gene. 2008, 408: 112-123. 10.1016/j.gene.2007.10.023.View ArticlePubMedGoogle Scholar
- Sheffield NC, Song H, Cameron L, Whiting MF: A comparative analysis of mitochondrial genomes in Coleoptera (Arthropoda: Insecta) and genome descriptions of six new beetles. Mol Biol Evol. 2008, 25: 2499-2509. 10.1093/molbev/msn198.PubMed CentralView ArticlePubMedGoogle Scholar
- Roberti M, Bruni F, Polosa PL, Gadaleta MN, Cantatore P: The Drosophila termination factor DmTTF regulates in vivo mitochondrial transcription. Nucleic Acids Res. 2006, 34: 2109-2116. 10.1093/nar/gkl181.PubMed CentralView ArticlePubMedGoogle Scholar
- Roberti M, Polosa PL, Bruni F, Musicco C, Gadaleta MN, Cantatore P: DmTTF, a novel mitochondrial transcription termination factor that recognises two sequences of Drosophila melanogaster mitochondrial DNA. Nucleic Acids Res. 2003, 31: 1597-1604. 10.1093/nar/gkg272.PubMed CentralView ArticlePubMedGoogle Scholar
- Dowton M, Cameron SL, Dowavic JI, Austin AD, Whiting MF: Characterization of 67 mitochondrial tRNA gene rearrangements in the Hymenoptera suggests that mitochondrial tRNA gene position is selectively neutral. Mol Biol Evol. 2009, 26: 1607-1617. 10.1093/molbev/msp072.View ArticlePubMedGoogle Scholar
- Macey JR, Larson A, Ananjeva NB, Fang ZL, Papenfuss TJ: Two novel gene orders and the role of light-strand replication in rearrangement of the vertebrate mitochondrial genome. Mol Biol Evol. 1997, 14: 91-104. 10.1093/oxfordjournals.molbev.a025706.View ArticlePubMedGoogle Scholar
- Lavrov DV, Boore JL, Brown WM: Complete mtDNA sequences of two millipedes suggest a new model for mitochondrial gene rearrangements: Duplication and nonrandom loss. Mol Biol Evol. 2002, 19: 163-169. 10.1093/oxfordjournals.molbev.a004068.View ArticlePubMedGoogle Scholar
- Hixson JE, Wong TW, Clayton DA: Both the conserved stem-loop and divergent 5'-flanking sequences are required for initiation at the human mitochondrial origin of light-strand DNA replication. J Biol Chem. 1986, 261: 2384-2390.PubMedGoogle Scholar
- Sheffield NC, Song H, Cameron SL, Whiting MF: Nonstationary evolution and compositional heterogeneity in beetle mitochondrial phylogenomics. Syst Biol. 2009, 58: 381-394. 10.1093/sysbio/syp037.View ArticlePubMedGoogle Scholar
- Song H, Sheffield NC, Cameron SL, Miller KB, Whiting MF: When phylogenetic assumptions are violated: base compositional heterogeneity and among-site rate variation in beetle mitochondrial phylogenomics. Syst Entomol. 2010, 35: 429-448. 10.1111/j.1365-3113.2009.00517.x.View ArticleGoogle Scholar
- Ma C, Liu C, Yang P, Kang L: The complete mitochondrial genomes of two band-winged grasshoppers, Gastrimargus marmoratus and Oedaleus asiaticus. BMC Genomics. 2009, 10: 156-10.1186/1471-2164-10-156.PubMed CentralView ArticlePubMedGoogle Scholar
- Benson G: Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1999, 27: 573-580. 10.1093/nar/27.2.573.PubMed CentralView ArticlePubMedGoogle Scholar
- Lowe TM, Eddy SR: tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997, 25: 955-964.PubMed CentralView ArticlePubMedGoogle Scholar
- Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22: 4673-4680. 10.1093/nar/22.22.4673.PubMed CentralView ArticlePubMedGoogle Scholar
- Feijao PC, Neiva LS, de Azeredo-Espin AML, Lessinger AC: AMiGA: the arthropodan mitochondrial genomes accessible database. Bioinformatics. 2006, 22: 902-903. 10.1093/bioinformatics/btl021.View ArticlePubMedGoogle Scholar
- Lobry JR: Properties of a general model of DNA evolution under no-strand-bias conditions. J Mol Evol. 1995, 40: 326-330. 10.1007/BF00163237.View ArticlePubMedGoogle Scholar
- Zuker M: Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31: 3406-3415. 10.1093/nar/gkg595.PubMed CentralView ArticlePubMedGoogle Scholar
- Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011, 28: 2731-2739. 10.1093/molbev/msr121.PubMed CentralView ArticlePubMedGoogle Scholar
- Jukes TH, Cantor CR: Evolution of protein molecules. Mammalian protein metabolism. Edited by: Munro H. 1969, New York: Academic Press, 21-132.View ArticleGoogle Scholar
- Robinson M, Gouy M, Gautier C, Mouchiroud D: Sensitivity of the relative-rate test to taxonomic sampling. Mol Biol Evol. 1998, 15: 1091-1098. 10.1093/oxfordjournals.molbev.a026016.View ArticlePubMedGoogle Scholar
- Robinson-Rechavi M, Huchon D: RRTree: Relative-Rate Tests between groups of sequences on a phylogenetic tree. Bioinformatics. 2000, 16: 296-297. 10.1093/bioinformatics/16.3.296.View ArticlePubMedGoogle Scholar