The complete mitochondrial genome of the citrus red mite Panonychus citri (Acari: Tetranychidae): high genome rearrangement and extremely truncated tRNAs
© Yuan et al; licensee BioMed Central Ltd. 2010
Received: 20 June 2010
Accepted: 23 October 2010
Published: 23 October 2010
The family Tetranychidae (Chelicerata: Acari) includes ~1200 species, many of which are of agronomic importance. To date, mitochondrial genomes of only two Tetranychidae species have been sequenced, and it has been found that these two mitochondrial genomes are characterized by many unusual features in genome organization and structure such as gene order and nucleotide frequency. The scarcity of available sequence data has greatly impeded evolutionary studies in Acari (mites and ticks). Information on Tetranychidae mitochondrial genomes is quite important for phylogenetic evaluation and population genetics, as well as the molecular evolution of functional genes such as acaricide-resistance genes. In this study, we sequenced the complete mitochondrial genome of Panonychus citri (Family Tetranychidae), a worldwide citrus pest, and provide a comparison to other Acari.
The mitochondrial genome of P. citri is a typical circular molecule of 13,077 bp, and contains the complete set of 37 genes that are usually found in metazoans. This is the smallest mitochondrial genome within all sequenced Acari and other Chelicerata, primarily due to the significant size reduction of protein coding genes (PCGs), a large rRNA gene, and the A + T-rich region. The mitochondrial gene order for P. citri is the same as those for P. ulmi and Tetranychus urticae, but distinctly different from other Acari by a series of gene translocations and/or inversions. The majority of the P. citri mitochondrial genome has a high A + T content (85.28%), which is also reflected by AT-rich codons being used more frequently, but exhibits a positive GC-skew (0.03). The Acari mitochondrial nad1 exhibits a faster amino acid substitution rate than other genes, and the variation of nucleotide substitution patterns of PCGs is significantly correlated with the G + C content. Most tRNA genes of P. citri are extremely truncated and atypical (44-65, 54.1 ± 4.1 bp), lacking either the T- or D-arm, as found in P. ulmi, T. urticae, and other Acariform mites.
The P. citri mitochondrial gene order is markedly different from those of other chelicerates, but is conserved within the family Tetranychidae indicating that high rearrangements have occurred after Tetranychidae diverged from other Acari. Comparative analyses suggest that the genome size, gene order, gene content, codon usage, and base composition are strongly variable among Acari mitochondrial genomes. While extremely small and unusual tRNA genes seem to be common for Acariform mites, further experimental evidence is needed.
The family Tetranychidae (spider mites) (Chelicerata: Acari) includes ~1200 species, many of which are of agronomic importance , such as Tetranychus urticae, Panonychus citri, and P. ulmi; the former is a worldwide pest of many plant species including several economically important agricultural crops, while the latter two are important fruit plant (e.g., apple and citrus) pests. Spider mites are often difficult to manage because of their ability to rapidly develop resistance to various acaricides . It has been reported that the resistance of T. urticae to the acaricide bifenazate is highly correlated with the remarkable mutations in the mitochondrial encoded cytochrome b (cob) . In addition, several acaricides, such as acequinocyl, fluacrypyrim , and METI-acaricides (mitochondrial electron transfer inhibitors, e.g., fenpyroximate and pyridaben) , which are now in widespread use globally, target mitochondrial proteins. Unravelling and comparing mitochondrial genomes of spider mites will not only increase our understanding of the molecular evolution of acaricide-resistance genes, but also help to develop new acaricides uniquely targeting mitochondrial genes.
During the last 10 years, arthropod mitochondrial genomes have been extensively sequenced due to the improvements of genomic technologies and the interest in mitochondrial genome organization and evolution . Mitochondrial genome sequences not only contain more information than the shorter sequences of single genes, but also provide larger data sets of genome-level features such as gene rearrangements and RNA secondary structures [6–8]. To date, the complete mitochondrial genomes have been sequenced from 25 Acari species. Among these, 14 species belong to the superorder of Parasitiformes while the remaining 11 species belong to the superorder of Acariformes. Most mitochondrial genomes are about 15 kb circular molecules and encode 37 genes including 13 protein-coding genes (PCGs), two rRNA genes (rRNAs), and 22 tRNA genes (tRNAs), which is typical of Metazoa . However, the mitochondrial genomes of Leptotrombidium pallidum and Metaseiulus occidentalis possess duplicated genes [10, 11], and the mtDNA of the sexual oribatid mite Steganacarus magnus lacks 16 tRNA genes . In addition, gene rearrangement, reverse base composition, and atypical tRNA genes are frequently present in Acari, especially for the Acariformes, such as in the mite genera Leptotrombidium[10, 13], and Dermatophagoides[14, 15], and also in the mite species P. ulmi and T. urticae.
Generally, mitochondrial gene content and gene order are highly conserved at the lower taxonomic rank (i.e. family and genus), but gene content variation and arrangement have reported for the genera Leptotrombidium[10, 13] and Dermatophagoides[14, 15]. In addition, the inference of mite mitochondrial tRNA genes may be extremely difficult and even error prone, especially when comparative data is absent . Thus, more mitochondrial genomes from closely related species will improve the accuracy of annotations for mitochondrial genomes, which will also greatly improve our understanding of molecular evolution and phylogenetic relationships [16–19]. In this study, we sequenced and analyzed the complete mitochondrial genome of the citrus red mite P. citri (Family Tetranychidae), an important citrus pest with a worldwide distribution, and provide a comparison to other Acari.
Results and discussion
Genome content and organization
The largest non-coding region, which presumably functions as the mitochondrial control region, is 57 bp long and is present between cox1 and nad3 (Figure 1, Additional File 1). This region is completely comprised of adenines and thymines (A + T-rich region) and is the third smallest among all sequenced mitochondrial genomes within Acari; only those of P. ulmi (55 bp) and T. urticae (44 bp) are slightly smaller (Figure 2). The maximum size difference found in the A + T-rich regions across all sequenced Acari mitochondrial genomes is 2,756 bp, indicating that strong size variation among Acari mitochondrial genomes is significantly correlated to the A + T-rich regions (Figure 2). This result is concordant with previous findings from other chelicerates  and insects [22–24]. In fact, the A + T-rich region has been identified as the source of size variation in the entire mitochondrial genome, usually due to the presence of a variable copy number of repetitive elements . The relative location of the A + T-rich region also varies greatly among Acari with the ancestral pattern of arthropods being between rrnS and trnI.
So far, the complete mitochondrial genomes of 26 species belonging to Acari have been sequenced and they exhibit great variation of gene order (Additional file 3). Among them, 7 of the 14 species belonging to the superorder of Parasitiformes (e.g. Ixodes spp.) share the same gene order as the ancestral chelicerates, while all of the 12 species belonging to the superorder of Acariformes are highly rearranged [14, 33], suggesting that these gene arrangements within Acari are independently derived . The rearrangement events (translocations and/or inversion) from other Acari (compared to L. polyphemus) do not seem to be more parsimonious to produce the gene arrangement of P. citri (Additional File 3). It is clear that the unique mitochondrial genome arrangement present in P. citri, P. ulmi, and T. urticae likely occurred after Tetranychidae diverged from other Acari, or after Acariformes split from Parasitiformes and Opilioacariformes, because this feature is not shared with any other Acari. Rearrangements of the mitochondrial genome should be relatively rare events at the evolutionary scale, and, therefore, provide a powerful tool to delimit deep divergences among some metazoan lineages . However, the mitochondrial gene rearrangement phenomenon seems to occur frequently and independently in Acari mitochondrial genomes [8, 33], possibly restricting the phylogenetic applications in recovering the evolutionary relationships between superorders within the Acari. On the other hand, gene order appears to be linked to taxonomic relatedness at the lower rank (i.e. genus, family). For example, the relationship between prostriate ticks and metastriate ticks can be distinguished by gene arrangements [31, 37].
Base composition and codon usage
Metazoan mitochondrial genomes usually present a clear strand bias in nucleotide composition [38, 39]. In detail, the J-strand is biased in favour of adenine and cytosine, while the N-strand consequently contains more thymine and guanine. The strand bias can be measured as AT- and GC-skews . The average AT-skew of Acari mitochondrial genome is 0.000 ± 0.101, ranging from -0.253 in Dermatophagoides farinae to 0.264 in Walchia hayashii, whereas the P. citri mitochondrial genome exhibits a slight AT-skew (0.071) (Figure 5). The marked AT-skew values are shared by the mitochondrial genomes of D. farinae (-0.253), D. pteronyssinus (-0.199), Unionicola foili (0.201), and W. hayashii (0.264).
The average GC-skew of Acari mitochondrial genome is -0.126 ± 0.195 and most of GC-skew values are negative, similar to those typically found in most metazoan mitochondrial genomes. However, as has been reported for other arthropods [38, 39, 41–43], six mite species in four genera are characterized by a reversal of GC-skew: Dermatophagoides[14, 15], Phytoseiulus, Varroa, and Panonychus (Figure 5). This reversal of the strand bias could be the result of inversion of the control region , which contains all initiation sites for replication and transcription of the mtDNA . Therefore, an inversion of the control region is expected to produce a global reversal of asymmetric mutational constraints in the mtDNA, with time resulting in a complete reversal of strand compositional bias . In the P. citri mtDNA most genes encoded on the J-strand show a positive GC-skew at the fourfold degenerate third codon position which is inverted to the common pattern and probably indicates a reversal of the control region (Additional file 1). Furthermore, this reverse strand bias may occur after the genus Panonychus split from the family Tetranychidae, because T. urticae, belonging to the same-family (Tetranychidae) with P. citri and P. ulmi, shows a usual GC-skew (negative), as found in most of Acari.
Codon usage for the 13 mitochondrial proteins of Panonychus citri
Ala (A )
The total length of all the 13 PCGs is 10,196 bp, and accounts for 77.97% of the entire length of P. citri mitochondrial genome (Additional file 1). The overall A + T content of PCGs is 73.91%, ranging from 78.45% (cox1) to 92.06% (nad6). All the PCGs start with ATN codons, which is typical for metazoan mitochondria : one (cox1) with ATC, three (nad3, nad4L, and nad1) with ATA, four (cox2, cox3, atp6, and nad4) with ATG, and the other five with ATT (Additional file 1). Eight PCGs terminate with the conventional stop codons TAA (cox1, nad3, nad4L, atp6, cox2, nad2, and nad4) or TAG (cob), whereas the remaining five have incomplete stop codons T. The presence of an incomplete stop codon is common in metazoan mitochondrial genomes  and these truncated stop codons are presumed to be completed via post-transcriptional polyadenylation . A comparison of codon numbers across the sequenced Acari mitochondrial genomes shows that all PCGs are highly variable in length, covering a range from 3,389 bp in P. citri to 6,328 bp in M. occidentalis (Figure 2). Notably, the M. occidentalis mitochondrial genome has the largest number of codons within chelicerates due to the duplication of many PCGs, even though nad3 and nad6 are lost . However, a recent study has found that the M. occidentalis mtDNA is smaller than originally suggested, and nad3 is not lacking but is in fact located between nad4L and rrnS. P. citri, P. ulmi, and T. urticae have a reduction in mean content of 19.8, 19.8, and 19.0 codons per PCG, respectively, making them the three smallest mitochondrial genomes within Acari.
Transfer and ribosomal RNA genes
The two genes encoding the large and small rRNA subunits (rrnL and rrnS) are located between trnE and trnR, and between trnY and trnG (Figure 1, Additional file 1). Both genes are encoded on the J-strand, as in P. ulmi, T. urticae, M. occidentalis, and Phytoseiulus persimilis, and in the two genera Dermatophagoides[14, 15] and Leptotrombidium (but L. pallidum has a duplicated rrnL gene on the N-strand) [10, 13]. In contrast, in the mitochondrial genomes of other Acari and most species of chelicerates and arthropods, both rRNA genes are encoded on the N-strand [12, 31, 33, 34, 43, 47, 53, 54]. We annotate the 5'- and 3'-ends of two rRNA genes as the first nucleotide downstream and upstream of corresponding tRNA genes, respectively, and the size of the rrnL and rrnS of P. citri are 989 bp and 648 bp long, respectively (Additional file 1). The A + T contents of rrnL and rrnS (86.66% and 87.54%, respectively) are similar to those of P. ulmi (86.76% and 88.01%, respectively) and T. urticae (85.27% and 85.91%, respectively), but much higher than the average value of Acari (78.58 ± 4.57% and 77.17 ± 5.08%, respectively). The boundaries of some tRNA genes are incorrectly delimited in P. ulmi, T. urticae and another strain of P. citri (see below). This aspect affects the boundaries of rrnL and rrnS in these taxa. Thus we re-annotate also these genes (Additional file 2). The size of rrnL and rrnS of P. citri is similar to those of another P. citri strain (992 bp and 650 bp), P. ulmi (983 bp and 659 bp) and T. urticae (992 bp and 645 bp). The size of rrnL of P. citri is the second shortest among all sequenced Acari mitochondrial genomes, whereas the size of rrnS is slightly larger than those of other Acariform mites (637.83 ± 27.70 bp), but are much shorter than those found in the Parasitiformes (702.57 ± 21.52 bp) (Figure 2).
Out of 22 tRNA genes usually present in metazoan mitochondrial genomes, only 13 tRNA genes can be detected in the P. citri mitochondrial genome by tRNAscan-SE  and/or ARWEN . The remaining nine tRNA genes (trnN, trnD, trnP, trnY, trnS2, trnA, trnS1, trnV, trnI) were identified by manually aligning unassigned sequences to known tRNA genes from T. urticae and P. ulmi, as suggested by Masta and Boore . All 22 tRNA sequences were aligned with those of P. ulmi and T. urticae, and show high similarity among Tetranychidae, especially for the anticodon stem (Additional file 7). However, only eight tRNA genes (trnF, trnY, trnT, trnL2, trnC, trnH, trnW, and trnM) of both P. ulmi and T. urticae are correctly annotated on GenBank. Among the remaining tRNA genes, the boundaries of ten tRNA genes of another P. citri strain (trnR, trnP, trnG, trnT, trnQ, trnC, trnA, trnS1, trnV, and trnI) and T. urticae (trnN, trnD, trnE, trnP, trnG, trnQ, trnS2, trnA, trnV, and trnI), and 11 tRNA genes of P. ulmi (trnN, trnL1, trnR, trnP, trnK, trnQ, trnS2, trnA, trnS1, trnV, and trnI) were incorrect on GenBank (Additional file 2), because most of them appear to lack the sequences to form the canonical amino acid acceptor stem (seven nucleotides) or at least one D- or T-arm (Additional file 8). The trnK of P. ulmi is misannotated on the J-strand, but in this location an unpaired anticodon stem is found. In fact, the majority of the nucleotides of trnK among Tetranychidae are highly conserved (Additional file 7), and only when trnK of P. ulmi is on the N-strand, as in P. citri and T. urticae, can canonical secondary structure of tRNA genes be found (Additional file 8). Therefore, we re-annotate these tRNA genes to incorporate the conserved structural features of tRNA genes (e.g., the possession of seven nucleotides in the amino acid acceptor stem, and at least one T- or D-arm) (Additional file 2), and present their secondary structures in Additional file 8.
Out of 22 tRNA genes, only three tRNA genes (trnN, trnL2, and trnK) can potentially fold into a typical cloverleaf structure, whereas all the remaining 19 tRNA genes appear to lack the sequence to code the D- or T-arm (Figure 9), as found in P. ulmi and T. urticae (Additional file 8). In at least 13 tRNA genes, the T-arm has been substituted by a loop of variable size (TV-replacement), whereas another six tRNA genes (trnD, trnE, trnQ, trnS1, trnS2, and trnV) show a D-replacement loop instead of the D-arm (Figure 9). With the exception of trnP, which seems to be lost the D-arm in P. ulmi, all tRNA genes have similar secondary structures among Tetranychidae (Figure 9, Additional file 8). The loss of the D-arm in trnS1 (AGN) has been considered a typical feature of metazoan mitochondrial genomes . The absence of the T-arm seems to be a common feature for the tRNA genes of chelicerates from the orders of the Araneae, Scorpiones, Thelyphonida, and Acariform Acari [10, 13–15, 43, 57], whereas other orders (Amblypygi, Opiliones, Solifugae, and Parasitiform Acari) possess typical metazoan cloverleaf tRNAs . On the other hand, the loss of the D-arm of tRNA genes is an uncommon circumstance but has been reported for a few of mitochondrial tRNA genes from chelicerates, including the scorpion Centruroides limpidus, the sea spiders Nymphon gracile and Achelia bituberculata, and five mites belonging to two genera Leptotrombidium[10, 13] and Dermatophagoides. It has been shown that in the nematode Ascaris suum the tRNA genes that lack either the D- or T-arm are functional , but functional tRNA genes that lack both the D- and T-arms have not been found before. However, tRNA genes that lack both T- and D-arms have been reported for the sea spider A. bituberculata (trnA)  and the scorpion C. limpidus (trnQ and trnS1) . In the American house dust mite D. farinae, some tRNA genes (e.g. trnA) lacking the D-arm have a small (2-3 bp) and thermodynamically unstable T-arm, suggesting that these tRNA genes may have lost both D- and T-arms in reality . In this study, we also found that some inferred T-arms (e.g., trnS2, trnV) or D-arms (e.g., trnY, trnR, trnP) were short (Figure 9). In particular, the inferred D-arm of trnY in P. ulmi and T. urticae (only one bp) is shorter than in P. citri, whereas the D-arm of trnP is lost in P. ulmi, casting doubt on their identity as D-arms. Therefore, further experiments are needed to investigate whether these truly tRNA genes lack both D- and T-arms and if so, whether they are functional.
Twenty of 22 tRNA genes have a five bp well-paired anticodon stem, and the remaining two tRNA genes (trnM and trnS1) have a single mismatch within this stem. All tRNA genes, but trnI, have the seven canonical nucleotides in the anticodon loop, whereas trnI has eight nucleotides in this region, which is also found for trnI of P. ulmi and T. urticae (Additional file 8). These noncanonical anticodon loops are not common, but have also been reported for the house dust mite D. pteronyssinus (trnL2) , the scorpion Mesobuthus gibbosus (trnH and trnN) , and the wild two-humped Camelus bactrianus ferus (trnS1) . Only nine of the 22 tRNA genes have a completely matched seven bp aminoacyl acceptor stem (trnN, trnD, trnE, trnG, trnL2, trnK, trnF, trnW, and trnY), while the remaining 13 tRNA genes have 1-3 bp mismatches in this stem. This type of a mis-paired acceptor stem seems to be a common phenomenon for tRNA genes of chelicerates (e.g., Araneae [42, 43], Acari [14, 15], Scorpiones ), and a posttranscriptional RNA editing mechanism has been proposed to maintain function of these tRNA genes [43, 61].
We sequenced the complete mitochondrial genome of the spider mite, P. citri (Family Tetranychidae). This mitochondrial genome in size is similar to those of other spider mites, P. ulmi and T. urticae, and is the smallest among all sequenced Acari and other Chelicerate genomes. The gene order of the P. citri mtDNA is identical to those of P. ulmi and T. urticae, but markedly differs from those of other chelicerates by a large number of gene inversions and/or translocations, suggesting that rearrangements occurred after Tetranychidae diverged from other Acari. Comparative analyses among Acari mitochondrial genomes show that the genome size, gene order, gene content, codon usage, and base composition are strongly variable. The Acari mitochondrial nad1 exhibits a faster amino acid substitution rate than the average, and the G + C content variation causes the different evolutionary patterns among genes of Acari mitochondrial genomes. Most tRNA genes present in P. citri are minimal and atypical, lacking the D- or T-arm, as found in P. ulmi and T. urticae. While extremely short and unusual tRNA genes seem to be common for Acariform mites, further experimental evidence is needed.
Samples and DNA extraction
Female adult of P. citri was collected on Trifoliate orange from Citrus Research Institute of Chinese Academy of Agricultural Sciences, Chongqing, China. Total DNA was extracted from about 800 females using a CTAB-based protocol  and stored at -20°C.
PCR amplification and sequencing
Fourteen pairs of PCR primers were employed to amplify overlapping segments of the entire mitochondrial genome of P. citri. Initially, cox1 and cob genes were amplified using the primers COI-F/R [63, 64] and CB3-F/CB4-R , respectively. Four perfectly matching primers, namely cox1-R1, cox1-F4, cob-R3 and cob-F3, were designed on the basis of the sequence information from cox1 and cob. Other primers were designed based on the conserved nucleotide sequences in T. urticae and P. ulmi (GenBank: NC_012571). A full of list of primers as well as PCR conditions are presented in Additional file 10. All PCR products were separated by electrophoresis on a 1% agarose gel, purified with DNA Gel Purification Kit (Watson, Shanghai), and cloned into the pGEM-T vector (Promega, USA). After heat-shock transformation of Escherichia coli (Trans5α, Beijing TransGen Biotech) cells, the positive recombinant clone with an insert was sequenced with M13 primers on both strands.
Sequence assembly, annotation and analysis
Sequence data were assembled using SeqMan software (DNAStar, Inc.). Protein coding genes (PCGs) were identified by ORF Finder implemented at the NCBI website with the invertebrate mitochondrial genetic codes and by comparison with the published Acari mitochondrial sequences with Clustal W 2.0 . Two large non-protein-coding regions were candidates for the rRNA genes (rrnL and rrnS). The boundaries were determined based on alignments and secondary structures of rRNA sequences of other mite species. The tRNA genes were identified by their cloverleaf secondary structure using tRNAscan-SE 1.21  and ARWEN . For tRNAscan-SE the following parameters were changed: Search Mode = "EufindtRNA-Cove", Source = "Nematode Mito", Genetic Code = "Invertebrate Mito" and Cove score cutoff = 0.1. ARWEN was run with default parameters. Other tRNA genes were identified by aligning to known tRNA genes from P. ulmi and T. urticae. The secondary structure models for two rRNA genes of P. citri were constructed by comparison with the published rRNA secondary structures for L. pallidum, D. pteronyssinus, and S. magnus. The secondary structure of A + T-rich region (putative control region) was constructed using Mfold Server . The complete mitochondrial genome sequence of P. citri has been deposited in the GenBank database under the accession number HM189212. The base composition, codon usage, and nucleotide substitution were analyzed with Mega 4.0  and DAMBE 5.0.59 . Mitochondrial genome sequences from other Acari and the horseshoe crab L. polyphemus were obtained for comparative analyses (see Additional file 11 for GenBank accession numbers).
- atp6 and atp8:
genes for the ATPase subunits 6 and 8
genes for cytochrome C oxidase subunits I-III
- cob :
a gene for apocytochrome b
- nad1-nad6 and nad4L:
genes for NADH dehydrogenase subunits 1-6 and 4L
- rrnL :
large (16S) rRNA subunit (gene)
- rrnS :
small (12S) rRNA subunit (gene)
- trnX (where X is replaced by one letter amino acid code of the corresponding amino acid):
We are grateful to five anonymous referees for providing invaluable comments and suggestions. We thank Dr. Helen Hull-Sanders and Stephen Sanders for critical reading of the manuscript. We also thank Mr. Fei Lu and Chen-Xiao Hu for the technical assistance in genome sequencing. This study was supported in part by a Special Fund for Agro-scientific Research in the Public Interest (nyhyzx07-057), the Program for Changjiang Scholars and Innovative Research Team in University (IRT0976), Natural Science Foundation of Chongqing (CSTC, 2009BA1042), and the earmarked fund for Modern Agro-industry (Citrus) Technology Research System of China to Jin-Jun Wang.
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