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Original Paper
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Acta Biochim Biophys
Sin 2008, 40: 7�18 |
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doi:10.1111/j.1745-7270.2008.00375.x |
Complete mitochondrial genome of Oxya chinensis (Orthoptera, Acridoidea)
Chenyan Zhang and Yuan Huang*
School of Biological Sciences, Shaanxi
Normal University, Xi'an 710062, China
Received: May 8,
2007�������
Accepted: September
27, 2007
This work was
supported by grants from the National Natural Science Foundation of China (No.
30470238 and 30670279)
*Corresponding
author: Tel, 86-29-85308451; Fax, 86-29-85310546; E-mail, [email protected]
The complete sequence of Oxya chinensis
(O. chinensis) mitochondrial� genome is reported here. It is 15,443 bp
in length and contains 75.9% A+T. The protein-coding genes have a similar A+T
content (75.2%). The initiation codon of the cytochrome oxidase subunit I gene
in the mitochondrial genome of O. chinensis appears to be ATC, instead
of the tetranucleotides that have been reported in Locusta migratoria (L.
migratoria) mitochondrial genome. The sizes of the large and small
ribosomal RNA genes are 1319 and 850 bp, respectively. The transfer RNA genes
have been modeled� and showed strong resemblance to the dipteran transfer�
RNAs, and all anticodons are identical to those of dipteran. The A+T-rich
region is 562 bp, shorter than that of other known Orthoptera insects. The six
conserved domains were identified within the A+T-rich region by comparing its
sequence with those of other grasshoppers. The result of phylogenetic analysis
based on the dataset containing 12 concatenated� protein sequences confirms the
close relationship of O. chinensis with L. migratoria.
Keywords������� mitochondrial DNA; strand asymmetry; codon usage; A+T-rich region; Oxya chinensis
Metazoan mitochondrial DNA (mtDNA) is typically a circular� molecule
between 14 and 18 kb in size that encodes� 37 genes: 13 protein-coding genes,
two ribosomal RNA (rRNA) genes, and 22 transfer RNA (tRNA) genes [1]. It has a
control region, named the A+T-rich region in insect, that contains the
replication origin of H-strand in vertebrates� and the replication origin of
two strands in Drosophila species [2].
Recently, amplification of the whole mitochondrial genome� using a long-range PCR technique has become an alternative approach for mtDNA purification and cloning, because of its feasibility in small animals and the availability� of standard molecular biology laboratory facilities. Advances� in DNA sequencing technology make it possible to determine longer sequences for large numbers of taxa. The complete mtDNA sequences from numerous metazoan� species have been reported to date [3], such as fishes [4], birds [5], cockroach, and dragonfly [6].
The growing interest in phylogenetic reconstruction of the mitochondrial genome has triggered a rapid increase in the number of published complete mitochondrial genome sequences [7]. The number of mtDNA sequences determined� from vertebrates is larger than those from insects, despite the fact that insects represent the largest number of animal species. Until now, more than 1015 complete metazoa mitochondrial genomes have been reported (http://www.ncbi.nlm.nih.gov). Of these, 58 are from insects, but only two are in Orthoptera, Locusta migratoria (L. migra�toria) [8] and Gryllotalpa orientalis (G. orientalis) [9].
The Orthoptera, belonging to hemimetabolous insects, is composed of more than 20,000 species. Several conflicting� hypotheses on the phylogenetic position of the Orthoptera have been proposed, but they have not been well supported by experimental evidence [10,11]. More mitochondrial genomes might help to resolve the phylogenetic relationships of orthopteran insects.
Oxya chinensis (Orthoptera: Acridoidea: Catantopidae) is one of the most common and widely distributed grasshoppers� in China, and is a serious pest of maize, sorghum, wheat, and especially rice. Some partial mtDNA of O. chinensis sequences have been published in GeneBank (http://www.ncbi.nlm.nih.gov/GeneBank), but the complete mtDNA sequence has not yet been available. Here we report the complete mtDNA sequence of O. chinensis and its annotated results.
Materials and Methods
Sample and DNA extraction
An adult specimen of O. chinensis was collected from Chang�an (Shaanxi, China). After an examination of external� morphology for identification, the specimen was stored at -80 �C. Total genomic DNA was extracted from the muscle of one of the specimen�s femurs by the standard proteinase� K and phenol/chloroform extraction method, then stored at -20 �C [12].
Long-range PCRs
The whole mitochondrial genome was amplified in two large overlapping fragments by long-range PCRs, using the primer pairs LP03 with LP04, and LP05 with LP06 (Table 1). Long-range PCRs were carried out in a thermal cycler MyCycler 580BR 3007 (Bio-Rad, Hercules, USA). Reactions were carried out with 25 ml reaction volume containing 3.7 ml sterile distilled H2O, 2.5 ml of 10�Long and Accurate PCR buffer (TaKaRa, Dalian, China), 4 ml dNTP (2.5 mM), 2.5 ml MgCl2 (25 mM), 3.5 ml each primer (10 mM), 0.3 ml of 2.5 U Long and Accurate (TaKaRa), and 5 ml template (10 mM). Cycle parameters included an initial denaturation step of 93 �C for 2 min; 40 cycles of 92 �C for 10 s; 52.5 �C for 8 min 30 s; and terminated with an extension at 68 �C for 7 min. Each PCR reaction yielded a single amplicon that was detected in 1% (W/V) agarose gels with ethidium bromide staining.
Short-range PCRs
Amplicons were purified by a DNA gel extraction kit (U-gene Biotechnology, Hefei, China) according to the supplier�s instructions, then used as templates for subsequent� short-range PCRs. Twenty-nine pairs of PCR primers were designed according to aligned mitochondrial genomes of 12 insect species in seven hemimetabolic orders, and these primers were used to amplify short overlapping� segments of the entire mitochondrial genome of O. chinensis. Detailed information about primers used in this study is shown in Table 1. Short-range PCRs were done in the thermal cycler MyCycler 580BR 3007 and reactions� were carried out in 25 ml reaction volume containing� 14.9 ml sterile distilled H2O, 2.5 ml PCR buffer (TaKaRa), 2 ml dNTP (2.5 mM), 2.5 ml MgCl2 (25 mM), 1 ml each primer (10 mM), 0.1 ml Z-Taq polymerase (TaKaRa), and 1 ml template (diluted long-range PCR products). The thermal cycle profile was as follows: denaturation� at 94 �C for 2 min; 30 cycles of 94 �C for 30 s, 38-55 �C for 30 s, and 70 �C for 90 s; and the final elongation was carried out at 72 �C for 7 min.
Sequencing
Short-range PCR products were purified using the DNA gel extraction kit, and sequencing reactions were conducted using dye-labeled terminators (BigDye terminator V3.1; Applied Biosystems, Foster City, USA). Primers used in sequencing were the same as those used in short-range PCRs. The fragments that could not be sequenced very well using PCR primers were cloned into PMD18-T vector� (TaKaRa), and then the resulting plasmid DNA was sequenced. All products were sequenced on an ABI Prism 3100 sequencer (Applied Biosystems).
Sequence assembly and annotation
Sequences were assembled with Sequencing Analysis (Applied Biosystems) and Staden Package version 1.5 software� [13]. The location of protein-coding genes and rRNA genes was identified by comparing them with those in the L. migratoria mitochondrial genome. The majority of the tRNA genes were recognized by tRNAscan-SE version� 1.21 [14], and the remaining tRNA genes were identified by inspecting sequences with tRNA-like secondary� structures and anticodons. The A+T-rich region� was determined by aligning the sequences with homologous� regions in other grasshoppers� mitochondrial genome sequences� using ClustalX version 1.83 [15].
The complete mitochondrial genome sequence of O. chinensis is available through the National Center for Biotechnology� Information nucleotide database under the accession number EF437157.
Phylogenetic analysis
Phylogenetic analysis was carried out based on 10 complete� mitochondrial genomes of polyneoptera insect species: Periplaneta fuliginosa (NC006076), Tamolanica tamolana (DQ241797), L. migratoria (NC001712), G. orientalis (NC006678), Gampsocleis gratiosa (unpublished data from our laboratory, 2007), O. chinensis (EF437157), Sclerophasma paresisensis (DQ241798), Timema californicum (DQ241799), Grylloblatta sculleni (DQ241796), and Pteronarcys princeps (AY687866). Each of the 13 protein sequences from 10 selected species was aligned with ClustalX version 1.83. ATP8 was discarded because it is too short in length and highly variable in phylogenetic� analysis. The remaining 12 aligned protein sequences were edited manually with BioEdit version 7.0 [16], then concatenated to a single amino acid sequence dataset. This dataset was analyzed using the Maximum likelihood (ML) and Bayesian inference (BI) methods. The ML method was carried out using TreeFinder [17] with the mtArt+G(4) model [18] and bootstrap analysis with 100 replicates. The BI method was carried out using MRBAYES version 3.1.2 [19] with the following options: four independent Markov chains, 150,000 generations, tree sampling every 10 generations, and a burn-in of 15,000 trees produced at the initial stage.
Results and Discussion
Genome structure and organization
The entire mitochondrial genome of O. chinensis is 15,443 bp long, 279 bp smaller than that of L. migratoria, 78 bp larger than that of G. orientalis, but well within the size range of most insects (14-19 kb). The sequence encodes 37 typical metazoan genes (13 protein-coding genes, 22 tRNAs, two rRNAs) and an A+T-rich region (Fig. 1). There are 11,218 bp in protein-coding regions, 1471 bp in tRNAs, 1318 bp in large rRNA, 850 bp in small rRNA, and 562 bp in the A+T-rich region. The order of tRNALys and tRNAAsp in the mitochondrial genome of O. chinensis and L. migratoria is different from the hypothesized ancestral� arthropod.
The O. chinensis mitochondrial genome has 14 overlapping� genes. The total length of overlapping fragments� is 65 bp with length varying from 1 to 19 bp (Table 2). The longest overlap occurs between cytochrome� oxidase subunit III and tRNAGly (19 bp). There are 5 bp overlaps between ATPase subunit 8 (ATP8) and ATP6, and 7 bp between NADH dehydrogenase subunit 4 (ND4) and ND4L. In agreement with a previous study, ATP6 and ND4L overlap with their own immediate upstream� genes ATP8 and ND4, respectively. Overlaps between ATP8 and ATP6 in all known mtDNA of arthropods are 7 bp, except that of Apis mellifera (A. mellifera) [20]. It has been suggested that the mRNAs of ATP6 and ND4L, if alone, might be too short to be translated� efficiently. But this does not seem to be imperative for all animals. Recently, transcriptional mapping analysis in several� animal species revealed the presence of bicistronic transcripts for both the ATP8-ATP6 and the ND4-ND4L gene pairs [21]. Gene overlaps might be resolved by gene expression, such as mRNA translation and/or processing mechanisms in animal mitochondria [22].
The O. chinensis mitochondrial genome has 17 intergenic spacers in a total of 87 bp with length varying in 1-21 bp. The longest intergenic spacer in the mitochondrial genome of O. chinensis, L. migratoria, and G. orientalis locates between tRNASer(UCN) and ND1, and it might suggest that some control elements locate in this spacer in Orthoptera insects. Also there is a 193 bp intergenic spacer between tRNASer(UCN) and ND1 in the mitochondrial genome of A. mellifera, thought to be functional as another origin of replication.
Base composition
The nucleotide composition of the O. chinensis mitochondrial genome is biased toward adenine and thymine (75.9%) (Table 3). This corresponds well to the AT bias generally observed in insect mitochondrial genomes, which range from 69.5% in Triatoma dimidiata to 84.9% in A. mellifera. The A+T content of protein-coding genes is 75.2%, lower than that of many other insects. The strongest� AT bias is found in the third codon position (91.1%) and the A+T-rich region (86.8%). The A+T content� of the first codon positions (68.8%) and the second� codon positions (65.8%) are lowest in the mitochondrial genome of O. chinensis.
The total A+C content of L-strand DNA in O. chinensis is 56.3%, lower than the 59.1% found in L. migratoria. The A+C content of protein-coding genes of O. chinensis is 44.2%, well concordant with ranges from 43.3% to 45.6% in other insect species. As for the AT-skew, the A content is higher than T in rRNA genes, tRNA genes, and the A+T-rich region. The situation is the opposite in protein�-coding genes. As for the GC-skew, the C content is higher than G in rRNA genes, tRNA genes, and the A+T-rich region, while G content is higher than C in protein-coding genes. Although the exact reason for strand asymmetry� in mtDNA is unknown, one possible reason is the accumulation� of mutations on different strands, caused by strands being displaced during the replication cycle [23].
Protein-coding genes
Translation initiation and termination signals��� All O. chinensis protein-coding genes typically have ATN as the initiation codon. ATG is the most used initiation codon (eight genes), then ATT (two), ATC (two), and ATA (one) (Table 2). The initiation codon of the cytochrome oxidase subunit I (COI) gene has been extensively discussed in several arthropod species including insects [24]. Tetranucleotides (ATAA, TTAA, and ATTA) and a hexanucleotide (ATTTAA) were postulated as the initiation� codon of the COI gene, but the initiation codon of the COI gene in O. chinensis is the typical trinucleotide ATC.
The protein-coding genes take TAA (nine) and TAG (three) as termination codons, except the ND5 gene (Table 2). The ND5 gene has the incomplete termination codon T, also found in L. migratoria and G. orientalis. The in�complete termination codon is commonly found in metazoan� mitochondrial genomes, and the reasonable interpretation� is that mRNA polyadenylation makes complete� TAA stop codon [25].
Codon usage� ��There are different nucleotide frequencies in all codon positions between the two strands. In the H-strand, the frequencies of nucleotides are A>T>G>C at the first codon position, A>T>C>G at the third codon position, and T>A>C>G at the second codon position (Fig. 2). In the L-strand, frequencies of nucleotides are T>A>G>C at the first and third codon position, and T>A>C>G at the second codon position. Despite an overall lower A+T content in protein-coding genes, the content of T is the highest compared with that of rRNA genes, tRNA genes, A+T-rich region. The higher content of T in the second position might be related to a preference for non-polar and hydrophobic amino acids in membrane-associated proteins [26]. At the third codon, the least frequent� nucleotide is G in the H-strand and C in the L-strand, probably reflecting the mutation pattern in the mitochondrial genome, as nucleotides at the third codon position are under the least selective pressure [27].
The mtDNA codon usage is strongly influenced by base composition. The strands of O. chinensis mtDNA with different AT-skews and GC-skews cause different patterns of codon usage on the two strands (Table 3). According to Lavrov et al [20], we divided all amino acids (except Leu and Ser, which are encoded by two families of codons) into three types, �AC-rich� (with A or C in both first and second codons: H, K, N, P, Q, T), �GT-rich� (with G or T in both first and second codons: C, F, G, V, W) and �neutral� (E, I, M, R, Y). The ratio of AC-rich codons to GT-rich codons on the H-strand is 1.1:1, 1.2:1, and 1.1:1 in O. chinensis, L. migratoria, and G. orientalis, respectively. The ratio of GT-rich codons to AC-rich codons on the L-strand is 2.00:1, 2.11:1, and 2.21:1 in O. chinensis, L. migratoria, and G. orientalis, respectively. The proportion of neutral codons on the H-strand and the L-strand are similar in O. chinensis, L. migratoria, and G. orientalis. These data show that GT-rich amino acids preferentially� locate on the L-strand.
tRNA and rRNA genes
There are 22 tRNA genes in O. chinensis, all of which have the typical clover leaf structure, except tRNASer(AGN) that lacks the dihydrouracil arm [28] (Fig. 3). A total of 28 mismatched base pairs occur in the tRNAs of O. chinensis. Of these, 16 are G-U pairs, and the remaining 12 are U-U, C-C, A-A, A-G, and A-C mismatches. The total numbers of mismatches in 22 tRNA genes found in G. orientalis and Cepaea nemoralis is 34 and 25, respectively. Most mismatches in O. chinensis locate at the 3� region of the acceptor stem and D-stem. Tomita et al [29] showed that mismatches in the 3� region of the acceptor stem of tRNA genes can be corrected by RNA editing, but the reason for high numbers of mismatches in the D-stem is unclear. Boore et al noted that overlaps between tRNAs is corrected� by polyadenylation, but there is not an exact explanation of how polyadenylation takes place in tRNA processing [30].
The boundaries of rRNA genes were determined by sequence� alignment with that of L. migratoria. The large and small ribosomal RNA genes are 1319 and 850 bp in length, respectively, with an A+T content of 78.60% and 76.59%, respectively. The secondary structure models of the two mitochondrial ribosomal subunits are important for understanding probabilities of nucleotide substitutions, and evaluating the reliability of phylogenetic reconstructions. Domain III of the 12S rRNA gene and domains IV and V of the 16S rRNA gene are highly conserved in insects. The secondary structure of domain III of 12S rRNA of O. chinensis is modeled through comparison with that of Gomphocerippus rufus (Z93247) [31], and the secondary structure of domains IV and V of 16S rRNA of O. chinensis is modeled by comparison with that of Ateliacris annulicornis [32] (Fig. 4).
A+T-rich region
The A+T-rich region of the O. chinensis mitochondrial genome locates between small rRNA and tRNAIle. This region is 562 bp long with 86.8% A+T content, shorter than that of both L. migratoria (875 bp) and G. orientalis (920 bp), but average when compared with that of insects. The variation in length and number of units is responsible for the size variation of the A+T-rich region. Zhang and Hewitt [33] found eight blocks while studying the AT-rich regions of Ateliacris annulicornis and Schistocerca gregaria. They also noted that the control regions in insects� can be classified into two different groups: group 1 contains two different domains, one conserved with a putative replication region, and the other variable, such as in Drosophila; group 2 contains some short conserved structure elements that scatter over the whole region, such as in some grasshoppers.
Here, comparing the A+T-rich region of O. chinensis with that of three other grasshoppers, L. migratoria, Schistocerca gregaria, and Chorthippus parallelus [34], six conserved domains (Blocks A, B, D, E1, E2, and F) were found (Fig. 5). Block A is a polyT stretch near tRNAIle, and it might be involved in the control of transcription and/or replication initiation. Blocks B and D are AT-rich domains. Block B overlaps with Block C in many positions, so Block C is not shown here. Block B resembles the stop signals of D-loop synthesis in human and mouse mtDNA. Block D is not conserved in O. chinensis. Blocks E1 and E2 are conserved domains in insects, and the two forms a highly conserved stem-loop structure that is potentially associated with the origin of L-strand replication. Zhang and Hewitt found �TATA� in the 5� region and �G(A)nT� in the 3� region, but we did not find �G(A)nT� in the 3� region, only CAT near the 3� region. The secondary structure� is shown in Fig. 6. Block F is a conserved GA-rich domain adjacent to 12S rRNA, and the content of G in this block is 20%, much higher than in the A+T-rich region (5%). There is a large gap between Blocks D and E1 compared with other insects, the main reason for such a short A+T-rich region in O. chinensis.
Phylogenetic analysis
The ML and BI methods generated phylogenetic trees with the same topology (Fig. 7). O. chinensis and L. migratoria are sister groups, supported strongly by both ML and BI analysis. Two Caelifera species (O. chinensis and L. migratoria) are more closely related with G. orientalis than with Gampsocleis gratiosa in both ML and BI trees, opposite to traditional opinion. The monophyly of Orthoptera is supported in both trees, but has low bootstrapping support in the ML tree. Morphological and recent molecular biology studies clearly support a monophyly of the Orthoptera [35]. But several authors have questioned the monophyly of the Orthoptera and proposed a paraphyletic relationship between Ensifera and Caelifera [36]. To further understand the phylogenetic relationship of Orthoptera, a larger number of orthopteran species need to be examined.
�
Conclusion
The complete sequence of the O. chinensis mitochondrial genome is 15,443 bp in length and contains 75.9% A+T. The sequence encodes the 37 typical metazoan genes (13 protein-coding genes, 22 tRNAs, two rRNAs and an A+T-rich region). There are 11,218 bp in protein-coding regions, 1471 bp in tRNAs, 1318 bp in large rRNA, 850 bp in small rRNA, and 562 bp in the A+T-rich region. The initiation codon of the COI gene appears to be ATC. There exist a total of 65 bp overlaps of varying lengths, from 1 to 19 bp, between 14 genes, and 87 bp intergenic spacers, with lengths varying between 1 and 21 bp, between� 17 genes. The six conserved domains were identified within the A+T-rich region by comparing their sequences with those of other grasshoppers. The result of phylo�genetic analysis based on the dataset of 12 concatenated protein sequences confirms the sister relationship of O. chinensis with L. migratoria, but the monophyly of four orthopteran species was not well supported in the ML tree.
Acknowledgement
We thank Dr. Huimeng Lu (Shaanxi Normal
University, Xi�an, China) for the design of primers and discussion during the
experiments.
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