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Article

Mitochondrial Genome Characteristics Reveal Evolution of Acanthopsetta nadeshnyi (Jordan and Starks, 1904) and Phylogenetic Relationships

by
Li-min Yang
1,
Jing-feng Xue
2,
Xiao-man Zhao
2,
Ke Ding
3,4,
Zhao-wen Liu
1,2,
Zhou-si-yu Wang
1,
Jian-bing Chen
1 and
You-kun Huang
2,*
1
School of Materials and Environmental Engineering, Chizhou University, Chizhou 247000, China
2
Anhui Provincial Key Laboratory for Quality and Safety of Agri-Products, School of Resource and Environment, Anhui Agricultural University, Hefei 230036, China
3
State Key Laboratory of Mining Response and Disaster Prevention and Control in Deep Coal Mines, Anhui University of Science and Technology, Huainan 232001, China
4
State Key Laboratory for Geomechanics and Deep Underground Engineering, China University of Mining and Technology, Xuzhou 221116, China
*
Author to whom correspondence should be addressed.
Genes 2024, 15(7), 893; https://doi.org/10.3390/genes15070893
Submission received: 13 June 2024 / Revised: 2 July 2024 / Accepted: 4 July 2024 / Published: 8 July 2024
(This article belongs to the Special Issue Molecular Evolution, Mitochondrial Genomics and Mitochondrial Genome Expression in Animals—2nd Edition)
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Abstract

:
In the present study, the mitochondrial genomic characteristics of Acanthopsetta nadeshnyi have been reported and have depicted the phylogenetic relationship among Pleuronectidae. Combined with a comparative analysis of 13 PCGs, the TN93 model was used to review the neutral evolution and habitat evolution catalysis of the mitogenome to verify the distancing and purification selectivity of the mitogenome in Pleuronectidae. At the same time, a species differentiation and classification model based on mitogenome analysis data was established. This study is expected to provide a new perspective on the phylogenetic relationship and taxonomic status of A. nadeshnyi and lay a foundation for further exploration of environmental and biological evolutionary mechanisms.

1. Introduction

The data analysis of mitogenome is a fundamental indicator for analyzing the relationship between vertebrate evolution and phylogeny [1]. In recent years, these studies have provided a clearer positioning of species status on the ecological chain as more and more complete mitochondrial genome information is being reported [2,3]. Generally, the mitogenome structure of vertebrates is arranged in a specific order [4]. These components include 13 protein-coding genes (ATP6, ATP8, COX1-3, CytB, NAD1-6, and NAD4L), 2 ribosomal ribonucleic acids (rrnS and rrnL), and 22 transfer RNA genes (tRNAs) [5]. These characteristic information contain crucial information for molecular evolution, such as base composition bias, codon usage, and substitution rate [6]. In addition, the mitogenome with simple structures and low recombination levels exhibits more gene copies with fewer bases, making it widely used in the study of biological evolutionary origins and genetic diversity [7,8].
A. nadeshnyi (Jordan and Starks, 1904) (Acanthopsetta, Pleuronectiformes) is a species of ray-finned fish in the family of right-eye flounders. It is distributed in the northwest Pacific region, including the Korean Peninsula, Japan, and the Bering Sea [9,10]. In Pleuronectiformes, there are many species, but the genetic information of the reported species is limited. Several studies on comparative genomics are not sufficient to clarify the complete phylogenetic relationships [11]. Therefore, the ecological location of the species is not clear and there is an urgent need to carry out the ecological positioning of A. nadeshnyi.
With the development of molecular sequencing, comparative genomic results can no longer be a single indicator of species classification, and more reports will apply evolutionary data theory to the biological status of species [2,12,13]. In previous studies, different gene fragments have created different trees, but the complete evolutionary classification of this species is not clear: Studies have constructed phylogenetic trees for COX1 and 16S rRNA of 10 species of Pleuronectiformes, but these two trees are not completely identical [14]; another study used the control region of the mitogenome as a sample to compare a different tree [15]. Ultimately, the incomplete mitogenome cannot exhibit consistent phylogenetic outcomes. A study reported the full length of the mitogenome sequences in A. nadeshnyi, but gene structure and evolutionary intervals have not been analyzed in conjunction with evolutionary trees unfortunately [16]. This situation leads to incomplete phylogenetic research and unclear ecological location of A. nadeshnyi. At the same time, the composition characteristics of the genome and the evolutionary trends of related species were analyzed, which will help to locate the ecological position of the species. In order to clarify the evolutionary relationships and states of species, we sequenced and assembled the entire mitochondrial gene of A. nadeshnyi. For the first time, the test of evolutionary divergence time provides a clearer elucidation of A. nadeshnyis’ phylogenetic relationship and taxonomic status in this study.

2. Materials and Methods

2.1. Sample Collection, DNA Extraction, and PCR Amplification and Sequencing

The specimen of A. nadeshnyi was obtained from the east side of the Yellow Sea (33°47′ 10″ N, 126°59′ 30″ E) on 15 August 2017. This specimen (carcass length: 32 cm, female) is deposited in the Laboratory of the Museum of Materials and Environmental Engineering (Zhaowen Liu, [email protected]), under voucher number AN2109073. The total genomic DNA was extracted using a modified phenol–chloroform method from the muscle tissue [3]. The sample was subjected to the Sanger sequencing method (Sangon Biotech, Shanghai, China), forming a circular mitochondrial genome. Design primers were based on published mitochondrial genomes and strictly amplified according to the requirements of the reagent kit (Takara, Beijing, China) (PrimeSTAR® Max DNA Polymerase) (Supplementary Table S1).

2.2. Sequence Analysis and Assembly and Mitochondrial Genome Annotation

The sequencing fragment was spliced into a complete circular DNA using the CodonCode Aligner 5.1.5 (CodonCode Corporation, Dedham, MA, USA). We annotated the complete genome using a MITOS online server and manually corrected the tRNA structure (Supplementary Figure S1) [17].

2.3. Amino Acid Composition and Nucleotide Substitution Saturation Index of PCGs

The relative synonymous codon usage (RSCU) values and codon numbers were calculated by MEGA 11 [18]. The nonsynonymous mutation rates (Ka), synonymous mutation rates (Ks), and Ka/Ks ratio for the PCGs were calculated in DnaSP 5 [19]. The nucleotide substitution saturation index of PCGs was calculated using DAMBE, and the substitution fitting model for the three codons was TN93 [20].

2.4. Relative Evolutionary Rate Analysis

Mitochondrial genomes from 25 species were aligned using MUSCLE v3.8.31 (https://drive5.com/muscle/, accessed on 23 March 2024) and concatenated into a super-gene for each species. Evolutionary rates were determined from these super-gene sets using the tpcv module in the LINTRE program [21].

2.5. Divergence Time Estimation

The divergence times were estimated based on Beast 2 [22] via the approximate likelihood calculation method of the MCMCtree program, with the following parameters: --Substitution Model GTR; --Site Heterogeneity Model γ; --Tree Prior Yule Process; --Length of chain 10,000,000; and --Echo state to screen every 1000. Fossil records acquired from the TimeTree website (http://www.timetree.org) were used to calibrate the divergence times. We used TVBOT as a graphic beautification tool (https://www.chiplot.online/tvbot.html, accessed on 25 March 2024) [23].

2.6. Phylogenetic Tree Construction

Twenty-three complete Pleuronectidae mitochondrial genomes were downloaded from GenBank (https://www.ncbi.nlm.nih.gov/genbank/, accessed on 26 March 2024) for phylogenetic studies (Table 1). Two Saccopharyngiformes species, Eurypharynx pelecanoides and Saccopharynx lavenbergi, were selected as the outgroup. At the same time, in order to distinguish species and families, we set up the Acipenser dabryanus with a close relationship (Table 1). In the analysis, 13 PCG sequences were selected in order to construct a phylogenetic tree using MEGA 11 [18]. Ambiguous sequences were eliminated using Gblock v0.91 (Castresana, 2000) [24]. The phylogenetic analyses were conducted utilizing the MrBayes 3.2.6 and PhyML80 v3.0 software, based on Bayesian inference (BI) and maximum likelihood (ML), respectively [25,26]. ML analysis uses bootstrap analysis (1000 repetitions) to verify the relative support levels [27]. The resulting phylogenetic trees were visualized using FigTree v. 1.4.4 and its tool (https://itol.embl.de) [28].

3. Results and Discussion

3.1. Characteristics, Structure, and Overlapping of the Mitogenomes

Compared to the traditional mitogenomes, the mitochondrial genome of A. nadeshnyi exhibits the same gene sequence [29]. The complete mitogenome sequence of A. nadeshnyi was 17,211 bp (GenBank accessions OQ791285) (Figure 1). The circular mitochondrial genome contained 13 PCGs, 2 rRNA genes (12S rRNA and 16S rRNA), 22 putative tRNA genes, and a control region (Dloop).
In the mitogenomes, most of the coding fragments were on the heavy strand. Among them, eight tRNAs (tRNA-Gln, tRNA-Ala, tRNA-Asn, tRNA-Cys, tRNA-Tyr, tRNA-Ser, tRNA-Glu, and tRNA-Pro) were on the light strand, and the other fourteen tRNAs were all on the heavy strand. The length of each tRNA ranged from 65 to 74 bp (Table 2), and they were able to form a stable clover structure (Supplementary Figure S1). The small coding subunit (12S rRNA) and large coding subunit (16S rRNA) appeared on both sides with tRNA-Phe and tRNA-Leu, which were located on the H-chain and separated by the tRNA-Val. They were 950 bp and 1714 bp lengths, respectively (Table 2). Except for ND6, all remaining CD areas were located on the heavy strand (Figure 1).

3.2. Protein-Coding Genes and Codon Usage

The total length of all PCGs was 10596 bp in the mitogenome of A. nadeshnyi, which accounted for 61.57% of the whole genome (Table 2). The comparison of the initiation of all PCGs showed that all CDs start with ATG as the starting codon, except for COX1 which was GTG. In terms of terminating codons, each CD was different: the COX2, ND3, ND4, and Cytb genes used an incomplete T stop codon; the COX3 gene used TA; the ND2 gene used TAG; and the ND1, COX1, ATP8, ATP6, ND4L, ND5, and ND6 genes used TAA.
In an RSCU analysis, different codon usage frequencies indicated the selection evolutionary pressure of different amino acids (Figure 2). Generally speaking, the codon composition of longer amino acids is more abundant [30]. In this study, Leu1, Ser 2, Pro, and Thr also showed greater abundance compared to other amino acids. Interestingly, Val, Arg, and Gly exhibited a higher abundance with fewer quantities. Therefore, among multiple amino acid frequencies, Val, Arg, and Gly might also have a more stable genetic efficiency [31]. On the other hand, other amino acids may undergo relatively unstable genetic evolution due to genetic mutations or random genetic drift. These unstable sites may choose better amino acid codons due to different environmental selection pressures [30].

3.3. Mitogenome Mutations and Evolutionary Relationships in Pleuronectidae

In the publicly available mitogenomes, we selected twenty-three typical genomes of Pleuronectidae for calculating the evolutionary selection pressure of A. nadeshnyi. Meanwhile, we set up species A. dabryanus with the same close relationship and species E. pelecanoides and S. lavenbergi with two distant relationships to verify the accuracy of the results mutually. Based on the gene sequences of 13 PCGs of the mitogenomes, the relative evolutionary pressure of each species could be characterized. As shown in the results (Figure 3A), the evolutionary pressure on E. jordani and E. pelecanoides was relatively low. In other species, most stress indices were around −0.15, and this might be related to the genetic stability of mitochondria [32]. The relatively similar mutation pressure index not only demonstrates the maternal heritability of the mitogenomes but may also indicate the similarity of environmental selection pressure [33]. In the analysis of synonymous mutations in amino acids, different Ka and Ks values exhibit relatively similar Ka/Ks values (Figure 3B). The difference in Ka values among different Pleuronectidae species was relatively small, which may indicate that the frequency of neutral evolution was relatively similar among different species, and this accumulation of neutral evolution may also lead to non-environmental selectivity of the mitogenomes [34]. In the evolutionary process of the Pleuronectidae species, constrained evolution and divergent evolution seemed to be closely related to gene mutations (Ka/Ks). In most evolution, evolutionary selection of the mitogenomes eliminates harmful gene mutations and maintains the stability of the original amino acids [35].
At the same time, we used TN93 as a model to verify the base substitution ratio and nucleotide frequency of the three codons (Figure 4) [36]. Generally speaking, the nonsynonymy of the second codon (Figure 4B) and the synonymy of the third codon (Figure 4C) jointly affect changes in amino acid evolution [37]. In the results of this study, Figure 4B,C exhibited different enrichment patterns; the common frequency of the first and second codons (Figure 4D) was similar to the frequency characteristics of the first codon (Figure 5), and nonsynonymous mutations may approach neutral mutations. This result was mutually consistent with the above inference (Ka/Ks) and was also supported by the purify selection theory [38].

3.4. Divergence Time and Phylogenetic Analysis

In recent years, divergence time estimation has become increasingly prominent in evolutionary biology [39]. Methodological and empirical advances now allow time trees to be estimated more accurately than ever before [26]. It is assumed that the molecular evolution rate of a species is approximately constant, that is, the evolution rate of genetic differences should be proportional to the time of differentiation (molecular clock) [40]. For any large molecule (DNA sequence or protein sequence), there is an approximately constant evolutionary rate across all evolutionary lineages [41]. If the number of mutations aggregated on an evolutionary branch is proportional to the length of independent evolution time of that branch, then its replacement rate may approximately maintain a constant value during the evolution process [42]. Generally speaking, an accurate estimation method is to use the fossil time of a specific group as a correction, and then estimate the divergence time between species based on the degree of divergence between gene sequences and molecular clocks [43]. We can simultaneously estimate the occurrence time of other nodes on the phylogenetic tree in order to infer the origin of related groups and the divergence time of different groups [41,43].
In this study, all PCGs of the mitochondrial basic groups of twenty-seven species were used as units for calculating the evolutionary time tree (Figure 5). The life evolution scale of Figure 5 is based on the relative divergence time of two outer groups E. pelecanoides and S. lavenbergi as a unit. Among them, the divergence time between E. pelecanoides and S. lavenbergi is 25.9–118.3 Mya, and 39 Mya is selected as the optimal unit scale based on species affinity (https//timetree.org). It was interesting that species under the same subject cluster to other subjects. The clustering of most species of Pleuronectidae was natural, except for A. stomias and E. jordani. In the topology of divergence time (Figure 5), the separation time of A. dabryanus (Acipenseridae) was approximately 297.78–340.32 Mya, but it clustered together with species from other families. This may be convergent evolution of A. dabryanus and P. cornutus or other species of Pleuronectidae in similar habitats [44]. Perhaps due to the environment at different latitudes, light, and temperature, A. stomias and E. jordani underwent a divergent evolutionary process. Unfortunately, the comparison of mitochondrial genomes alone cannot be the sole explanation for this phenomenon, and it was necessary to correctly verify the survival range of all species worldwide.
Except for the divergence time of the cross-clustering, all species exhibited consistency in divergence time and sequence tree construction (Figure 5) (Supplementary Figure S2). The tree construction of the two results showed almost similar clustering topology. A. nadeshnyi and D. rikuzenius differentiated over a period of 42.54 Mya during the Cenozoic (Figure 5), and similar conclusions were also reflected in the results of systematic development (Supplementary Figure S2). The differentiation time of Pleuronectidae was 42.54–340.32 Mya, and this may be related to the changes in Quaternary glacier movement [45,46,47]. Unfortunately, due to the ancient nature of the mitogenome, the results of gene tree construction may be different from those of the species tree.

4. Conclusions

In this study, we reported the complete mitochondrial genome of A. nadeshnyi, analyzed the corresponding genomic information, compared with the reported mitogenomes of A. nadeshnyi and congeneric species, and depicted the phylogenetic relationship among Pleuronectidae. Meanwhile, combined with a comparative analysis of 13 PCGs, the TN93 model was used to review the neutral evolution and environmental evolution catalysis of the mitochondrial genome to verify the distancing and purification selectivity of the mitochondrial genome in Pleuronectidae. A cross-analysis model for species differentiation and tracing was established using mitochondrial genome data using divergence time and phylogenetic analysis. In future research, more mitochondrial genome data will be made public, and this data model will be more accurate when combined with the historical changes in the coastline. This study provides basic data support for analyzing the genetic data features of A. nadeshnyi, while also providing a more theoretical basis for the evolutionary classification of Pleuronectidae.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/genes15070893/s1, Figure S1: The cloverleaf structure of 22 tRNAs in the mitochondrial genome of A.nadeshnyi; Figure S2: Phylogenetic tree of the Pleuronectidae inferred from the nucleotide sequences of 13 PCGs using the Bayesian inference (BI) and maximum likelihood (ML) methods. The numbers on the branches indicate: (1) Evolutionary Branch Length Values: phylogenetic relationships after species establishment, (2) Bootstrap: the confidence value of kinship distance; Table S1: PCR amplification steps; Table S2: PCR amplification primers.

Author Contributions

Conceptualization, L.-m.Y., J.-b.C. and Y.-k.H.; Methodology, L.-m.Y., J.-b.C. and Y.-k.H.; Software, L.-m.Y., J.-f.X., X.-m.Z., J.-b.C. and Y.-k.H.; Validation, J.-f.X., J.-b.C. and Y.-k.H.; Formal analysis, J.-f.X. and K.D.; Investigation, K.D., Z.-w.L., J.-b.C. and Y.-k.H.; Resources, Z.-w.L. and Z.-s.-y.W.; Data curation, X.-m.Z., Z.-w.L., Z.-s.-y.W., J.-b.C. and Y.-k.H.; Writing—original draft, L.-m.Y., J.-f.X., J.-b.C. and Y.-k.H.; Writing—review & editing, L.-m.Y., K.D., Z.-w.L., Z.-s.-y.W., J.-b.C. and Y.-k.H.; Visualization, X.-m.Z., J.-b.C. and Y.-k.H.; Supervision, K.D., Z.-w.L. and Z.-s.-y.W.; Project administration, K.D., Z.-w.L. and Z.-s.-y.W.; Funding acquisition, K.D., Z.-w.L., Z.-s.-y.W. and J.-b.C. All authors have read and agreed to the published version of the manuscript.

Funding

This work was under the financial aid of National Natural Science Foundation of China (52227901), the Natural Science Foundation of the Higher Education Institutions of Anhui Province (KJ2021A1132), the school-level key projects of Chizhou College (CZ2023ZRZ01, CZ2021ZRZ12) and the Natural Students’ Innovation and Entrepreneurship Training Program (202311306026, 202311306056, 202311306063).

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Board of Anhui Agricultural University (protocol code GBT 35823-2018 and 2 July 2021).

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available to researchers eligible under the Research Ethics Board rules on request from the corresponding author due to ethical restrictions.

Conflicts of Interest

The authors declare that no conflicts of interest.

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Genes 15 00893 g001
Figure 1. Gene map of A. nadeshnyi mitogenome.
Figure 1. Gene map of A. nadeshnyi mitogenome.
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Genes 15 00893 g002
Figure 2. The relative synonymous codon usage (RSCU) in the mitogenome of A. nadeshnyi (A). (The y-axis represents the usage frequency of the corresponding amino acid codons in 13 PCGs. Different colors represent the different codons in the amino acids.) The amino acid composition in the mitogenome of A. nadeshnyi (B). (The x- and y-axis refer to the amino acid composition and the number of each amino acid in 13 PCGs, respectively.)
Figure 2. The relative synonymous codon usage (RSCU) in the mitogenome of A. nadeshnyi (A). (The y-axis represents the usage frequency of the corresponding amino acid codons in 13 PCGs. Different colors represent the different codons in the amino acids.) The amino acid composition in the mitogenome of A. nadeshnyi (B). (The x- and y-axis refer to the amino acid composition and the number of each amino acid in 13 PCGs, respectively.)
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Genes 15 00893 g003
Figure 3. The relative evolutionary pressure index of species based on the mitochondrial genome model of Pleuronectidae (A). The ratio (Ks/Ks) of synonymous substitution (Ka) and synonymous substitution (Ks) calculated using amino acids as data points indicates the mutation pressure index of the mitochondrial genome (B).
Figure 3. The relative evolutionary pressure index of species based on the mitochondrial genome model of Pleuronectidae (A). The ratio (Ks/Ks) of synonymous substitution (Ka) and synonymous substitution (Ks) calculated using amino acids as data points indicates the mutation pressure index of the mitochondrial genome (B).
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Figure 4. Nucleotide substitution saturation plots for all 13 PCGs of Pleuronectidae. First codon positions (A); second codon positions (B); third codon positions (C); and first codon and second codon positions (D). Plots in blue and green indicate transition and transversion, respectively.
Figure 4. Nucleotide substitution saturation plots for all 13 PCGs of Pleuronectidae. First codon positions (A); second codon positions (B); third codon positions (C); and first codon and second codon positions (D). Plots in blue and green indicate transition and transversion, respectively.
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Genes 15 00893 g005
Figure 5. The divergence time and geological scale of species mitochondrial genomes of Pleuronectidae. The life evolution scale of this chart is based on the relative divergence time of two outer groups E. pelecanoides and S. lavenbergi as a unit. Among them, the divergence time between E. pelecanoides and S. lavenbergi is 25.9–118.3 Mya, and 39 Mya is selected as the unit scale based on species affinity (https://timetree.org).
Figure 5. The divergence time and geological scale of species mitochondrial genomes of Pleuronectidae. The life evolution scale of this chart is based on the relative divergence time of two outer groups E. pelecanoides and S. lavenbergi as a unit. Among them, the divergence time between E. pelecanoides and S. lavenbergi is 25.9–118.3 Mya, and 39 Mya is selected as the unit scale based on species affinity (https://timetree.org).
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Table 1. Species attribution and accession number.
Table 1. Species attribution and accession number.
SpeciesSpeciesFamilyOrderAccession No.
A. nadeshnyiA. nadeshnyiAcanthopsettaPleuronectidaeOQ791285
Atheresthes stomiasA. stomiasAtheresthesNC_083173
Cleisthenes herzensteiniC. herzensteiniCleisthenesNC_028021
Clidoderma asperrimumC. asperrimumClidodermaMK210570
D. rikuzeniusD. rikuzeniusDexistesNC_066467
Eopsetta jordaniE. jordaniEopsettaNC_083049
Glyptocephalus stelleriG. stelleriGlyptocephalusNC_060723
Hippoglossoides elassodonH. elassodonHippoglossoidesNC_082804
Hippoglossoides platessoidesH. platessoidesMN122825
Hippoglossoides robustusH. robustusNC_082769
Hippoglossus hippoglossusH. hippoglossusHippoglossusNC_009709
Hippoglossus stenolepisH. stenolepisNC_009710
Kareius bicoloratusK. bicoloratusKareiusNC_080271
Lepidopsetta bilineataL. bilineataLepidopsettaNC_083649
Limanda limandaL. limandaLimandaOY755015
Limanda sakhalinensisL. sakhalinensisNC_082768
Microstomus pacificusM. pacificusMicrostomusNC_082805
Parophrys vetulusP. vetulusParophrysOR482580
Platichthys stellatusP. stellatusPlatichthysNC_010966
Pleuronichthys cornutusP. cornutusPleuronichthysNC_022445
Pseudopleuronectes americanusP. americanusPseudopleuronectesNC_082555
Pseudopleuronectes herzensteiniP. herzensteiniNC_063673
Pseudopleuronectes yokohamaeP. yokohamaeNC_028014
Reinhardtius hippoglossoidesR. hippoglossoidesReinhardtiusNC_009711
A. dabryanusA. dabryanusAcipenserAcipenseridaeNC_036420
E. pelecanoidesE. pelecanoidesEurypharynxEurypharyngidaeAB046473
S. lavenbergiS. lavenbergiSaccopharynxSaccopharyngidaeAB047825
Table 2. Features of mitochondrial genomes of A. nadeshnyi.
Table 2. Features of mitochondrial genomes of A. nadeshnyi.
MitogenomePositionLengthAminoStart/StopIntergenic Region from to (bp) *Strand #
From/To(bp)AcidCodon
tRNA-Phe (F)16868 0H
12S RNA681017950 −1H
tRNA-Val (V)1018109073 0H
16S RNA109128041714 0H
tRNA-LeuUUA (L1)2807288074 2H
ND128813855975325ATG/TAA0H
tRNA-Ile (I)3861393070 5H
tRNA-Gln (Q)4000393069 −1L
tRNA-Met (M)4001406969 0H
ND2406951151047349ATG/TAG−1H
tRNA-Trp (W)5114518572 −2H
tRNA-Ala (A)5255518769 1L
tRNA-Asn (N)5329525773 1L
tRNA-Cys (C)5431536765 37L
tRNA-Tyr (Y)5500543368 1L
COX1550270611560520GTG/TAA1H
tRNA-SerUCA (S1)7132706271 0L
tRNA-Asp (D)7147721771 14H
COX272247914691230ATG/T6H
tRNA-Lys (K)7915798773 0H
ATP87989815616856ATG/TAA1H
ATP681478830684228ATG/TAA-10H
COX388309614785261ATG/TA-1H
tRNA-Gly (G)9615968672 0H
ND3968710035349116ATG/T0H
tRNA-Arg (R)100361010469 0H
ND4L101051040129799ATG/TAA0H
ND410395117751381460ATG/T−7H
tRNA-His (H)117761184570 0H
tRNA-SerAGC (S2)118461191267 0H
tRNA-LeuCUA (L2)119191198971 6H
ND511990138401851617ATG/TAA0H
ND61432113803519173ATG/TAA−38L
tRNA-Glu (E)143901432269 0L
Cyt b14395155351141380ATG/T4H
tRNA-Thr (T)155361560873 0H
tRNA-Pro (P)156781560871 −1L
Dloop15679172111533 0H
* Intergenic region: non-coding bases between the feature on the same line and the line below, with a negative number indicating an overlap. # H: heavy strand; L: light strand.
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Yang, L.-m.; Xue, J.-f.; Zhao, X.-m.; Ding, K.; Liu, Z.-w.; Wang, Z.-s.-y.; Chen, J.-b.; Huang, Y.-k. Mitochondrial Genome Characteristics Reveal Evolution of Acanthopsetta nadeshnyi (Jordan and Starks, 1904) and Phylogenetic Relationships. Genes 2024, 15, 893. https://doi.org/10.3390/genes15070893

AMA Style

Yang L-m, Xue J-f, Zhao X-m, Ding K, Liu Z-w, Wang Z-s-y, Chen J-b, Huang Y-k. Mitochondrial Genome Characteristics Reveal Evolution of Acanthopsetta nadeshnyi (Jordan and Starks, 1904) and Phylogenetic Relationships. Genes. 2024; 15(7):893. https://doi.org/10.3390/genes15070893

Chicago/Turabian Style

Yang, Li-min, Jing-feng Xue, Xiao-man Zhao, Ke Ding, Zhao-wen Liu, Zhou-si-yu Wang, Jian-bing Chen, and You-kun Huang. 2024. "Mitochondrial Genome Characteristics Reveal Evolution of Acanthopsetta nadeshnyi (Jordan and Starks, 1904) and Phylogenetic Relationships" Genes 15, no. 7: 893. https://doi.org/10.3390/genes15070893

APA Style

Yang, L. -m., Xue, J. -f., Zhao, X. -m., Ding, K., Liu, Z. -w., Wang, Z. -s. -y., Chen, J. -b., & Huang, Y. -k. (2024). Mitochondrial Genome Characteristics Reveal Evolution of Acanthopsetta nadeshnyi (Jordan and Starks, 1904) and Phylogenetic Relationships. Genes, 15(7), 893. https://doi.org/10.3390/genes15070893

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