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Research Article
Complete mitochondrial genomes of two catfishes (Siluriformes, Bagridae) and their phylogenetic implications
expand article infoRenyi Zhang‡, Lei Deng‡, Xiaomei Lv‡, Qian Tang‡
‡ Guizhou Normal University, Guiyang, China

Corresponding author: Renyi Zhang ( zhangrenyi@gznu.edu.cn )

Academic editor: Tihomir Stefanov
© 2022 Renyi Zhang, Lei Deng, Xiaomei Lv, Qian Tang.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Zhang R, Deng L, Lv X, Tang Q (2022) Complete mitochondrial genomes of two catfishes (Siluriformes, Bagridae) and their phylogenetic implications. ZooKeys 1115: 103-116. https://doi.org/10.3897/zookeys.1115.85249
ZooBank: urn:lsid:zoobank.org:pub:7A01B01B-92F7-469B-B2BE-81F1B9324D2F
Open Access

Abstract

The mitochondrial genome (mitogenome) has been widely used as a molecular marker to investigate phylogenetic analysis and evolutionary history in fish. However, the study of mitogenomes is still scarce in the family Bagridae. In this study, the mitogenomes of Tachysurus brachyrhabdion and T. gracilis were sequenced, annotated, and analyzed. The mitogenomes were found to be 16,532 bp and 16,533 bp, respectively, and each contained 37 typical mitochondrial genes, which are 13 protein-coding genes (PCGs), 22 tRNA genes, two rRNA genes, and a control region. All PCGs begin with the codon ATG, except for the cytochrome c oxidase subunit 1 (COI) gene, while seven PCGs end with an incomplete termination codon. All tRNA genes can fold into their typical cloverleaf secondary structures, except for tRNASer(AGY), which lacks the dihydrouracil arm. The Ka/Ks ratios for all PCGs are far lower than one. Phylogenetic analyses based on Bayesian inference (BI) and maximum likelihood (ML) showed that the two clades in Bagridae excluded Rita rita. The monophyly of Tachysurus supports previous research and the traditional classification that Leiocassis, Pseudobagrus, Pelteobagrus, and Tachysurus belong to one genus (Tachysurus). These findings provide a phylogenetic basis for future phylogenetic and taxonomic studies of Bagridae.

Keywords

bagrid catfish, mitogenome, phylogenetic analysis, Tachysurus brachyrhabdion, Tachysurus gracilis

Introduction

The family Bagridae, commonly known as bagrid catfish, is widely distributed in Asia and Africa, with about 225 species in 19 genera (Fricke et al. 2022). It is one of the most diverse and complicated groups within Siluriformes. Regan (1911) first promoted bagrid fishes as a single-family and named Bagridae, including two subfamilies: Chrysichthyinae and Bagrinae. Based on osteological features, Jayaram (1968) divided Bagridae into five subfamilies: Ritinae, Chiysichthyinae, Bagrinae, Bagroidinae, and Auchenoglaninae. In 1992, Mo (1992) divided the traditional bagrid catfishes into three monophyletic groups: Caroteidae, Austroglanididae, and Bagridae; the latter Bagridae contained two subfamilies, Ritinae and Bagrinae. In the past two decades, molecular phylogenetic studies showed that Bagridae is monophyletic, with only Rita excluded (Sullivan et al. 2006; Vu et al. 2018). However, the phylogenetic relationships between different genera of Bagridae are not well understood, such as the monophyly or the validity of Leiocassis, Pseudobagrus, Pelteobagrus, and Tachysurus. Recently, Leiocassis, Pseudobagrus, Pelteobagrus, and Tachysurus were classified into Tachysurus according to morphological analysis (Cheng et al. 2021; Shao et al. 2021).

Tachysurus brachyrhabdion Cheng, Ishihara & Zhang, 2008 was firstly named Pseudobagrus brachyrhabdion in 2008 (Cheng et al. 2008). It is mainly distributed in the Yuanjiang and Xiangjiang rivers, including the southwest of Hunan Province and the northeast of Guizhou Province in China. Tachysurus gracilis Li, Chen & Chan, 2005 was firstly named Pseudobagrus gracilis in 2005 (Li et al. 2005). It inhabits in the freshwater drainages of southern China. They are essential economic species of freshwater fishes in local areas.

Mitochondria are eukaryotic organelles that play essential roles in oxidative phosphorylation and other biochemical functions. Similar to other vertebrates, fish mitochondrial DNA (mtDNA) is a circular double-stranded molecule, and it is independent of the nuclear genome (Xiao and Zhang 2000). Fish mtDNA is generally small (15–18 kb), containing 13 protein-coding genes (PCGs), 22 transfer RNA (tRNA) genes, two ribosomal RNA (rRNA) genes, and a non-coding region (D-loop) (Brown 2008; Zhang and Wang 2018; Zhang et al. 2021). The mitochondrial genome has been used to study fish species identification, genome evolution, and phylogenetic studies because of the advantages of its small size, multiple copies, maternal inheritance, rapid evolution rate, and lack of introns (Boore 1999; Xiao and Zhang 2000; Zhang and Wang 2018; Zhang et al. 2021).

In this study, the mitochondrial genomes of two catfishes (T. brachyrhabdion and T. gracilis) were sequenced, assembled, and compared to reveal their evolutionary relationship. These mitochondrial genomes will provide a phylogenetic basis for future phylogenetic and taxonomic studies of Bagridae.

Materials and methods

Sample collection and DNA extraction

Specimens of T. brachyrhabdion and T. gracilis were collected from Jiangkou County (27°46'12"N, 108°46'56"E) and Liping County (26°17'51"N, 109°7'25"E), Guizhou, China, respectively. The samples were preserved in 95% ethanol and stored at -20 °C until DNA extraction. Specimens were recognized as T. brachyrhabdion and T. gracilis by traditional morphology. The voucher specimens were deposited in the fish specimen room, School of Life Science, Guizhou Normal University under the voucher numbers GZNUSLS201909001~006 and GZNUSLS201907029~030 for T. brachyrhabdion and GZNUSLS202005279 for T. gracilis. Specimens GZNUSLS201907029 and GZNUSLS202005279 were destroyed for the molecular analysis. Total genomic DNA was extracted from muscle tissues using a standard high salt method (Sambrook et al. 1989). The integrity of the genomic DNA was evaluated via 1% agarose gel electrophoresis, and the concentration and purity of DNA were measured using an Epoch 2 Microplate Spectrophotometer (Bio Tek Instruments, Inc, Vermont, USA).

PCR amplification and sequencing

The whole mitogenomes of Tachysurus species were amplified in overlapping PCR fragments using 13 primer pairs designed based on the mitogenome of T. brevicaudatus (GenBank accession number: NC_021393) by Primer Premier 5.0 software (Lalitha 2000) (Suppl. material 3). PCR amplification were performed as described previously (Zhang et al. 2021). The PCR products were fractionated by electrophoresis through 1% agarose gel electrophoresis. The lengths of fragments were determined by comparison with the DL2000 DNA marker (TaKaRa, Japan). The PCR products were sent to Sangon Biotech. Co., Ltd. (Shanghai, China) for sequencing.

Sequence analysis and gene annotation

After sequencing, the sequence fragments were edited and assembled using the SeqMan software of DNAStar (DNASTAR Inc., Madison, WI, USA) to obtain the complete mitogenome sequences. Assembled mitogenome sequences were annotated using the MitoAnnotator on the MitoFish homepage (Sato et al. 2018). tRNA genes and their secondary structures were predicted with MITOS (Bernt et al. 2013) and tRNAscan-SE 2.0 (Chan et al. 2021). The base composition, codon usage, and relative synonymous codon usage (RSCU) values were calculated using MEGA 6.0 (Tamura et al. 2013). Strand asymmetry was calculated using the following formulae: AT-skew = (A-T)/(A+T) and GC-skew = (G-C)/(G+C) (Perna and Kocher 1995). The ratio of nonsynonymous substitutions (Ka), synonymous substitutions (Ks), and evolutionary rates (Ka/Ks) of each PCG was calculated using DnaSP v. 6.0 (Rozas et al. 2017).

Phylogenetic analysis

For phylogenetic analysis, sequences of 32 bagrid catfishes were downloaded from GenBank. Additionally, Cyprinus carpio (NC_001606.1), Silurus asotus (NC_015806.1), Liobagrus andersoni (NC_032035.1), and L. styani (NC_034647.1) were used as outgroups. The species used in the analysis are listed in Suppl. material 4. The shared 13 concatenated PCGs were extracted and recombined to construct a matrix using PhyloSuite v.1.1.16 (Zhang et al. 2020). The 13 PCGs were aligned separately using MAFFT v.7.313 (Katoh and Standley 2013) and concatenated into a sequence matrix using PhyloSuite v.1.1.16 (Zhang et al. 2020). The optimal partitioning scheme and nucleotide sequence substitution model of each partition were estimated using PartitionFinder v.2.1.11 (Lanfear et al. 2017) with the Corrected Akaike information criterion (AICc) criteria and greedy algorithm. Bayesian inference (BI) analysis was performed using MrBayes v.3.2.6 (Ronquist et al. 2012) with the models determined by PartitionFinder (Lanfear et al. 2017). Two independent runs of four Markov Chain Monte Carlo (MCMC) chains (one cold chain and three heated chains) were performed for one million generations sampling every 100 generations. The first 25% of the generations was discarded as burnin, and the remaining trees were used to generate a majority rule consensus tree. Maximum likelihood (ML) analysis was carried out using IQ-TREE v.1.6.8 (Nguyen et al. 2015) with 10,000 bootstrap replicates using the ultrafast bootstrapping algorithm (Minh et al. 2013). The phylogenetic trees were visualized and edited using FigTree v1.4.2 (http://tree.bio.ed.ac.uk/software/figtree/).

Results

Genome structure, organization, and base composition

The entire mitogenome sequences of the two catfishes had lengths of 16,532 bp for T. brachyrhabdion and 16,533 bp for T. gracilis (GenBank accessions MW712739 and OM759888, respectively) (Fig. 1, Table 1). Both sequences contained 13 PCGs (ND1-6, COI-III, ND4L, ATP6, ATP8, and Cytb), 22 tRNA genes (one for each amino acid, two for Leucine and Serine), two rRNA genes (12S and 16S rRNA), and a non-coding region (D-loop) (Fig. 1, Table 1). Among these genes, one PCG and eight tRNA genes were encoded on the minority strand (L-strand), while another 28 genes were encoded on the majority strand (H-strand) (Fig. 1, Table 1).

Figure 1. 

Circular map of the two catfishes mitochondrial genomes.

Table 1.
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Organization of mitochondrial genome of T. brachyrhabdion (TB) and T. gracilis (TG). H refers to the majority strand and L refers to the minority strand. Position numbers refer to positions on the majority strand.

Gene Strand Nucleotide number Length (bp) Intergenic nucleotide Anticodon Start/Stop codons
TB TG TB TG Start Stop
tRNAPhe H 1–70 1–70 70 0 0 GAA
12S rRNA H 71–1023 71–1023 953 0 0
tRNAVal H 1024–1095 1024–1095 72 0 0 TAC
16S rRNA H 1096–2774 1096–2774 1679 0 0
tRNALeu (UUR) H 2775–2849 2775–2849 75 0 0 TAA
ND1 H 2850–3824 2850–3824 975 2 2 ATG TAG
tRNAIle H 3827–3898 3827–3898 72 -1 -1 GAT
tRNAGln L 3898–3968 3898–3968 71 -1 -1 TTG
tRNAMet H 3968–4037 3968–4037 70 0 0 CAT
ND2 H 4038–5082 4038–5082 1045 0 0 ATG T
tRNATrp H 5083–5153 5083–5153 71 2 2 TCA
tRNAAla L 5156–5224 5156–5224 69 1 1 TGC
tRNAAsn L 5226–5298 5226–5298 73 32 32 GTT
tRNACys L 5331–5397 5331–5397 67 0 0 GCA
tRNATyr L 5398–5468 5398–5469 71/72 1 1 GTA
COI H 5470–7020 5471–7021 1551 0 0 GTG TAA
tRNASer (UCN) L 7021–7091 7022–7092 71 4 4 TGA
tRNAAsp H 7096–7168 7097–7169 73 14 14 GTC
COII H 7183–7873 7184–7874 691 0 0 ATG T
tRNALys H 7874–7947 7875–7948 74 1 1 TTT
ATPase 8 H 7949–8116 7950–8117 168 -10 -10 ATG TAA
ATPase 6 H 8107–8789 8108–8790 683 0 0 ATG TA
COIII H 8790–9573 8791–9574 784 0 0 ATG T
tRNAGly H 9574–9647 9575–9648 74 0 0 TCC
ND3 H 9648–9996 9649–9997 349 0 0 ATG T
tRNAArg H 9997–10067 9998–10068 71 0 0 TCG
ND4L H 10068–10364 10069–10365 297 -7 -7 ATG TAA
ND4 H 10358–11738 10359–11739 1381 0 0 ATG T
tRNAHis H 11739–11808 11740–11809 70 0 0 GTG
tRNASer (AGY) H 11809–11875 11810–11876 67 3 3 GCT
tRNALeu (CUN) H 11879–11951 11880–11952 73 0 0 TAG
ND5 H 11952–13778 11953–13779 1827 -4 -4 ATG TAA
ND6 L 13775–14290 13776–14291 516 0 0 ATG TAA
tRNAGlu L 14291–14359 14292–14360 69 2 2 TTC
Cytb H 14362–15499 14363–15500 1138 0 0 ATG T
tRNAThr H 15500–15572 15501–15573 73 -2 -2 TGT
tRNAPro L 15571–15640 15572–15641 70 0 0 TGG
D-loop H 15641–16532 15642–16533 16533 892 0 0

The overall base composition for both species was very similar, 31.02% A, 27.05% T, 15.55% G, and 26.38% C for T. brachyrhabdion and 31.03% A, 27.14% T, 15.52% G, and 26.31% C for T. gracilis (Table 2). The third codon position of PCGs had the highest A+T content (65.75% for T. brachyrhabdion and 66.04% for T. gracilis), while the first codon position of PCGs had the lowest A+T content (49.00% for T. brachyrhabdion and 49.11% for T. gracilis) (Table 2). In addition, skew metrics of the mitogenomes showed positive AT-skew and negative GC-skew (Table 2), indicating that As and Cs were more abundant than Ts and Gs.

Table 2.
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Nucleotide composition of the mitochondrial genomes of T. brachyrhabdion (TB) and T. gracilis (TG).

Length(bp) A% T% G% C% A+T% AT-skew GC-skew
TB TG TB TG TB TG TB TG TB TG TB TG TB TG TB TG
genome 16532 16533 31.02 31.03 27.05 27.14 15.55 15.52 26.38 26.31 58.07 58.17 0.0683 0.0669 -0.2585 -0.2580
PCGs 11405 11405 28.94 28.99 29.13 29.25 15.37 15.30 26.56 26.46 58.07 58.24 -0.0032 -0.0045 -0.2668 -0.2673
1st codon position 3806 3806 27.06 27.17 21.94 21.94 25.49 25.35 25.51 25.54 49.00 49.11 0.1046 0.1065 -0.0005 -0.0036
2nd codon position 3806 3806 18.61 18.63 40.87 40.95 13.55 13.53 26.97 26.89 59.47 59.58 -0.3743 -0.3746 -0.3312 -0.3307
3rd codon position 3806 3806 41.17 41.17 24.59 24.87 7.05 7.00 27.19 26.95 65.75 66.04 0.2522 0.2467 -0.5880 -0.5876
rRNA 2632 2632 34.77 34.65 22.38 22.34 19.64 19.72 23.21 23.29 57.14 56.99 0.2168 0.2160 -0.0833 -0.0830
tRNA 1566 1567 29.12 29.16 28.10 28.33 22.48 22.34 20.30 20.17 57.22 57.50 0.0179 0.0144 0.0507 0.0511
D-loop region 892 892 31.28 31.17 31.39 31.17 13.79 13.90 23.54 23.77 62.67 62.33 -0.0018 0.0000 -0.2613 -0.2619

Protein-coding genes

The mitogenomes of T. brachyrhabdion and T. gracilis had one PCG (ND6) encoded on the L-strand and the remaining PCGs on the H-strand. Both mitogenomes had 11,405 bp coding for PCGs, accounting for 3627/3626 amino acids (Table 2, Suppl. material 5). Both species had very similar codon usage, with the most commonly used amino acids being Leu (13.81%, 13.87%), Ser (9.98%, 10.04%), and Ile (8.88%, 8.80%) (Suppl. material 5). The RSCU values of the mitogenomes of the two species are summarized in Fig. 2. All PCGs start with ATG except for COI, which used GTG. For these protein-coding genes, the most common stop codon was TAA, although ND1 used TAG and some used the incomplete stop codon T – or TA-.

Figure 2. 

Relative synonymous codon usage (RSCU) in the mitogenomes of the T. brachyrhabdion A and T. gracilis B.

To investigate the evolutionary patterns under different selective pressures among 13 PCGs in bagrid catfishes, the value of Ka/Ks was calculated for each PCG, respectively (Fig. 3). The gene (ATP8) exhibited the highest ratio of all the PCGs, whereas COI had the lowest ratio. However, the Ka/Ks ratios for all PCGs were far lower than one (Fig. 3).

Figure 3. 

Ka/Ks of each PCG from 33 bagrid catfishes mitogenomes (Rita rita was excluded).

Ribosomal, transfer RNA genes and control region

Both the T. brachyrhabdion and T. gracilis mitogenomes contained two rRNA genes: the large ribosomal RNA subunit (16S rRNA) and small ribosomal RNA subunit (12S rRNA). The 16S rRNA was located between tRNAVal and tRNALeu (UUR), and the 12S rRNA was located between tRNAPhe and tRNAVal. The 12S rRNA genes and the 16S rRNA genes of both mitogenomes were 953 bp and 1679 bp, respectively.

Twenty-one tRNA genes produced the typical cloverleaf secondary structure, while tRNASer (AGY) gene lacked the dihydrouracil (DHU) arm (Figs S1 and S2). The sizes of the tRNA genes ranged from 67 bp (tRNACys and tRNASer (AGY)) to 75 bp (tRNALeu (UUR)) in both T. brachyrhabdion and T. gracilis (Table 1).

The putative control regions were located between tRNAPro and tRNAPhe in the two bagrid catfishes. The control regions of T. brachyrhabdion and T. gracilis were 892 bp in size. The average A+T content of the CRs (62.33%–62.67%) was higher than that of the whole genomes, PCGs, rRNAs, or tRNAs (57.14%–58.24%) (Table 2).

Phylogenetic analysis

To determine the phylogenetic relationship between T. brachyrhabdion and T. gracilis in the Characidae, we selected the concatenated nucleotide sequences of the combined mitochondrial gene set (13 PCGs) from 34 bagrid catfishes. As shown in Fig. 4, the phylogenetic analysis of the two tree models (BI and ML) using the combined mitochondrial gene set well supported the tree topologies and yielded identical results. Phylogenetic analysis reveals bagrid catfishes could be separated into two clades excluding Rita rita (Hamilton, 1822) with strong support (Fig. 4). Clade I included Hemibagrus, Sperata, and Mystus (BS = 100%, PP = 100%). Clade II was only composed of Tachysurus (BS = 100%, PP = 100%). Several monophyletic clades of Tachysurus, Sperata, Mystus, and Liobagrus were strongly supported (Fig. 4). Nevertheless, the genus Hemibagrus was paraphyletic (Fig. 4). In addition, our phylogenetic trees showed that T. brachyrhabdion and T. gracilis clustered together forming a group.

Figure 4. 

Phylogenetic tree obtained from BI and ML analysis based on the 13 PCGs dataset. The numbers at the nodes separated by “/” indicate the posterior probability (BI) and bootstrap value (ML).

Discussion

Over the past two to three decades, mitochondrial genes and genomes have been frequently used in fish studies (Xiao and Zhang 2000; Brown 2008; Zhang and Wang 2018). In this study, the complete mitochondrial genomes of T. brachyrhabdion and T. gracilis were sequenced. The order and arrangement of the two mitogenomes were identical to that of other bagrid catfishes (Liang et al. 2014; Tian et al. 2016; Liu et al. 2019). The genomes had a total length of 16,532 bp and 16,533 bp, with A + T contents at 58.07% and 58.17%, respectively. These A + T biases were within the known range (56.37–59.80%) reported for mitochondrial genomes in closely related fishes (Tian et al. 2016; Liu et al. 2019).

Most of the PCGs of these two species had ATG as the start codon except COI that had GTG as the start codon. The COI gene usually uses GTG as the start codon in other fishes, such as Lateolabrax, Sinocyclocheilus multipunctatus, and Microphysogobio elongatus (Shan et al. 2016; Zhang and Wang 2018; Zhang et al. 2021). The PCGs of these two bagrid catfishes had an incomplete stop codon that was automatically filled by post-transcriptional polyadenylation (Ojala et al. 1981). This was a common character in metazoans mitogenomes (Shan et al. 2016; Jiang et al. 2019; Li et al. 2021). Twenty-one tRNA genes showed the typical cloverleaf secondary structure (Suppl. material 1, 2), while the tRNA-SerAGY gene lacked the dihydrouracil (DHU) arm as noted in other fish species (Zhang and Wang 2018; Zhang et al. 2021). The low Ka/Ks value for each PCG indicated that they were all under strong purifying selection. The DNA barcoding gene COI had the lowest evolutionary rate, consistent with the results observed from other fish groups (Sun et al. 2021; Yu et al. 2021).

Phylogenetic analysis revealed Bagridae was supported as a monophyletic group with Rita rita excluded (Fig. 4), which is consistent with previous phylogenetic studies (Sullivan et al. 2006; Vu et al. 2018). The phylogenetic tree suggested the classification of R. rita should be further revised and perfected. Clade I was composed of two monophyletic groups (Sperata and Mystus) and one paraphyletic group (Hemibagrus) (Fig. 4), which is consistent with the previous study of Liu et al. (2019). The traditional genera Leiocassis, Pseudobagrus, Pelteobagrus, and Tachysurus were not each monophyletic (Hardman 2005; Ku et al. 2007; Liu et al. 2019), but instead were grouped into Tachysurus as found in recent research (Cheng et al. 2021; Shao et al. 2021). Our results supported that the species in Leiocassis, Pseudobagrus, Pelteobagrus, and Tachysurus belong to the same genus, which by taxonomic priority should be Tachysurus. Thus, the current concept of Tachysurus includes the traditional genera Leiocassis, Pseudobagrus, Pelteobagrus, and Tachysurus. Due to limited sample size and molecular data, the phylogeny discussed in this research should be regarded as preliminary. The growing number of available mitogenomes will improve our understanding of the phylogeny and classification of bagrid catfish.

Conclusions

This study reported the complete mitochondrial genome sequences of two bagrid catfishes. The study showed that mitogenomes of Bagridae were conserved in structure, gene order, and nucleotide composition. Phylogenetic analysis confirmed that Bagridae is monophyletic group with Rita rita excluded and the traditional classification that Leiocassis, Pseudobagrus, Pelteobagrus, and Tachysurus belong to one genus.

Acknowledgements

This work was supported by the Joint Fund of the National Natural Science Foundation of China and the Karst Science Research Center of Guizhou Province (Grant No. U1812401), Guizhou Provincial Science and Technology Foundation (Qiankehejichu[2018]1113), Natural Science Foundation of Guizhou Educational Committee (QianjiaoheKY[2021]306) and the Undergraduate Research Training Program of Guizhou Normal University (DK2019A023).

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Supplementary materials

Supplementary material 1 

Figure S1. Predicted tRNA structures of Tachysurus brachyrhabdion

Renyi Zhang, Lei Deng1, Xiaomei Lv, Qian Tang

Data type: image

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (2.13 MB)
Supplementary material 2 

Figure S2. Predicted tRNA structures of Tachysurus gracilis

Renyi Zhang, Lei Deng1, Xiaomei Lv, Qian Tang

Data type: image

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (4.71 MB)
Supplementary material 3 

Table S1. Primers used for PCR

Renyi Zhang, Lei Deng1, Xiaomei Lv, Qian Tang

Data type:molecular data

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (18.36 kb)
Supplementary material 4 

Tables S2. Species, GenBank accession number and length of mitogenomes used in this study

Renyi Zhang, Lei Deng1, Xiaomei Lv, Qian Tang

Data type: molecular data

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (16.70 kb)
Supplementary material 5 

Table S3. Number of codons in T. brachyrhabdion (TB) and T. gracilis (TG) for mitochondrial PCGs

Renyi Zhang, Lei Deng1, Xiaomei Lv, Qian Tang

Data type: molecular data

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (18.97 kb)
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