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The complete mitochondrial genome of the hybrid grouper Epinephelus moara (♀)×Epinephelus tukula (♂), and phylogenetic analysis in subfamily Epinephelinae
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Zhentong Li1, 3, Yongsheng Tian2, 3, *, Meiling Cheng3, 4, Linna Wang2, 3, Jingjing Zhang1, 3, Yuping Wu3, 4, Zunfang Pang5, Wenhui Ma5, Jieming Zhai5
Acta Oceanologica Sinica | 2020, 39(12) : 65 - 75
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Acta Oceanologica Sinica | 2020, 39(12): 65-75
• Marine Biology •
The complete mitochondrial genome of the hybrid grouper Epinephelus moara (♀)×Epinephelus tukula (♂), and phylogenetic analysis in subfamily Epinephelinae
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Zhentong Li1, 3, Yongsheng Tian2, 3, *, Meiling Cheng3, 4, Linna Wang2, 3, Jingjing Zhang1, 3, Yuping Wu3, 4, Zunfang Pang5, Wenhui Ma5, Jieming Zhai5
Affiliations
  • 1 College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China
  • 2 Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266071, China
  • 3 Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
  • 4 College of Fisheries and Life Science, Dalian Ocean University, Dalian 116023, China
  • 5 Laizhou Mingbo Aquatic Co. Ltd., Laizhou 261400, China
Published: 2020-12-25 doi: 10.1007/s13131-020-1689-7
Outline
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The mitochondrial genome (mitogenome) of hybrid grouper Epinephelus moara (♀)×Epinephelus tukula (♂), a new hybrid progeny, can provide valuable information for analyzing phylogeny and molecular evolution. In this study, the mitogenome was analyzed using PCR amplification and sequenced, then the phylogenetic relationship of E. moara (♀)×E. tukula (♂) and 35 other species were constructed using Maximum Likelihood and Neighbor-Joining methods with the nucleotide sequences of 13 conserved protein-coding genes (PCGs). The complete mitogenome of E. moara (♀)×E. tukula (♂) was 16 695 bp in length, which contained 13 PCGs, 2 rRNA genes, 22 tRNA genes, a replication origin and a control region. The composition and order of these genes were consistent with most other vertebrates. Of the 13 PCGs, 12 PCGs were encoded on the heavy strand, and ND6 was encoded on the light strand. The mitogenome of the E. moara (♀)×E. tukula (♂) had a higher AT nucleotide content, a positive AT-skew and a negative GC-skew. All protein initiation codons were ATG, except for COX and ND4 (GTG), ATP6 (CTG), and ND3 (ATA). ND2, COXII, ND3, ND4 and Cytb had T as the terminating codon, COXIII’s termination codon was TA, and the remaining PCGs of that were TAA. All tRNA genes, except for the lacking DHU-arm of tRNASer (AGN), were predicted to form a typical cloverleaf secondary structure. In addition, sequence similarity analysis (99% identity) and phylogenetic analysis (100% bootstrap value) indicated that the mitochondrial genome was maternally inherited. This study provides mitogenome data for studying genetic, phylogenetic relationships and breeding of grouper.

Epinephelus moara (♀)×Epinephelus tukula (♂)  /  Epinephelus moara  /  Epinephelus tukula  /  mitochondrial genome  /  phylogeny
Zhentong Li, Yongsheng Tian, Meiling Cheng, Linna Wang, Jingjing Zhang, Yuping Wu, Zunfang Pang, Wenhui Ma, Jieming Zhai. The complete mitochondrial genome of the hybrid grouper Epinephelus moara (♀)×Epinephelus tukula (♂), and phylogenetic analysis in subfamily Epinephelinae[J]. Acta Oceanologica Sinica, 2020 , 39 (12) : 65 -75 . DOI: 10.1007/s13131-020-1689-7
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1 Introduction
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The mitochondrial is a semi-autonomous organelle that can replicate autonomously under the control of nuclear genes ranging from 15 to 20 kilobases in length (Boore et al., 1999), and contains 37 genes: 13 protein-coding genes (PCGs), 2 RNA (12S RNA and 16S RNA), 22 tRNAs, and 1 control region that contains the initial sites for mtDNA replication and RNA transcription. Compared to nuclear DNA, mitogenome are small and relatively simple, and have the characteristics of coding content conservation, maternal inheritance, rapid evolution, and low levels of intermolecular genetic recombination (Boore, 1999). Therefore, mitogenome has been widely used to molecular research, such as the identification of species, the analysis of molecular evolution, the study of population genetic structure, and the analysis of phylogenetics (Brown et al., 1979; Moritz et al., 1987; Ballard and Whitlock, 2004; Liu et al., 2013). The complete mitogenome of hundreds of vertebrates species have been determined from mammals (Anderson et al., 1981; Bibb et al., 1981; Peng et al., 2007), chicken (Liu et al., 2016) and fish (Chang et al., 1994). As for Epinephelinae fishes, the first complete grouper mitogenome that was sequenced was Leopard coral grouper (Plectropomus leopardus) (Zhu and Yue, 2008), and mitogenomes from more than 30 species have been published since then (Zhuang et al., 2010; Qu et al., 2012; Oh et al., 2012; Zhu et al., 2016).
Mitogenome sequencing can accurately reflect the variation of individual bases. It is the most sensitive and reliable genetic analysis method and one of the most widely used markers in molecular phylogeography (Avise, 2009). At present, research about the mitogenome of Epinephelinae species helps us understand the evolutionary relationship of them. The detail of their evolutionry relationships based on the mitogenome phylogenetic trees was consistent with that conventional morphology-based classification to some extent (Zhu and Yue, 2008; Gao et al., 2017). However, the mitogenome sequence of most Epinephelinae species was not available, which will limit our understanding of actual evolutionary relationships. Hybrids may provide more information leading to a more scientific classification (Gao et al., 2017). In the process of biological evolution, hybridization has an important influence on species formation (Wang, 2017). More and more examples of homoploid hybrid speciation were found, such as Gila seminudea (DeMarais et al., 1992) and Cottus sp. (Stemshorn et al., 2011). There are many species in subfamily Epinephelinae and most them are found in tropical and subtropical. By studying the mitochondria of hybrids to reveal the inherent genetic mechanism of species formation, which is of great significance to study the molecular phylogeography of subfamily Epinephelinae (Avise, 2009; Gao et al., 2017).
Hybridization can combine the advantageous traits of different species of fish, and provide so-called heterosis of hybrid progeny, which improves the viability and tolerance to the environment, as well as resolving issues around germplasm during culturing. Hybridization as an effective breeding method has been widely used in fish breeding, including grouper (James et al., 1999; Glamuzina et al., 2001). Grouper is an extremely diverse group of marine fish, providing abundant genetic materials for hybridization (Heemstra and Randall, 1993), such as Epinephelus moara (♀) × Epinephelus lanceolatus (♂) (Gao et al., 2017), E. fuscoguttatus (♀) × E. tulcula (♂) (Tian et al., 2019). Epinephelus moara and E. tukula, which both belong to Serranidae in the order Perciformes, are widely loved by consumers due to its delicious flavor. Both E. moara and E. tukula are mainly distributed in western Pacific region (Guo et al., 2004; Tian et al., 2019). Epinephelus moara has high market value, tolerance to high temperature and salt concentrations and high adaptability to aquaculture, while E. tukula possesses the merits of strong disease resistance and rapid growth. Therefore, the good traits of both groupers can be collected by hybridization. The grouper E. moara (♀)×E. tukula (♂) (EMET) were obtained by artificial insemination with E. moara as the female parent and E. tukula as the male parent (Fig. 1). As hybrid progeny, EMET have superior performance, such as high disease resistance, higher survival rate, and lower deformity rate. However, there have been no studies on E. moara (♀)×E. tukula (♂) mitochondrial sequences.
In this study, we present the complete sequence of the hybrid EMET mitogenome. The overall composition and organization of the EMET mitogenome was similar to the typical mitochondria structure in vertebrates. Further more, we verified that the mitogenome was maternally inherited through phylogenetic analysis. The EMET mitogenome provides a useful genomic resource for breeding hybrids in Epinephelinae.
2 Materials and methods
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2.1 Sample collection and DNA extraction
The groupers E. moara and E. tukula cultured at Laizhou Mingbo Aquatic Co., Ltd. (Shandong, China) were collected from the wild. The hybrid were obtained by artificial insemination with E. moara as the female parent and E. tukula as the male parent. Three hybrid (EMET 1, 2, 3), six month-old, and mean total length (23.0±0.7) cm, were sampled and the fin were rapidly conserved in absolute ethanol and kept at –20°C for DNA extraction. Total genomic DNA was extracted from EMET fins using the OMEGA tissue DNA extraction kit (OMEGA, USA) according to the manufacturer’s instructions. All experiments were followed the National Institutes of Health’s Guide for the care and use of laboratory animals.
2.2 PCR amplification and sequencing
The complete mitogenome of EMET 2 was amplified by PCR using 19 primer pairs (Table 1), which were designed using Primer Premier 5.0 based on the complete mitogenome of E. moara (GenBank: JQ518290). Primers were synthesized by Ruibiotech Co. Ltd. (Hefei, China). PCR reactions were conducted using a total volume of 30 μL consisting of 22.1 μL deionized H2O, 3 μL 10× PCR buffer (15 mmol/L Mg2+), 2.4 μL dNTPs (2.5 mmol/L), 1 μL DNA template (50 ng/μL), 0.3 μL ExTaq DNA polymerase (5 U/μL, Takara), 0.6 μL forward primer (10 μmol/L) and 0.6 μL reverse primer (10 μmol/L). The PCR reaction conditions were as follows: initial denaturation 95°C for 10 min, followed by 36 cycles of 95°C for 30 s, 58–59°C for 35 s, 72°C for 90 s, followed by final extension 72°C for 8 min and terminated at 4°C. The PCR products (5 μL) were separated by a 0.8% agarose gel electrophoresis and visualized under UV light (BIO-RAD, Italy). Sequencing of the samples were conducted by Ruibiotech Co. Ltd. (Hefei, China).
2.3 DNA sequence annotation and analysis
The circular mitogenome of EMET was assembled using the overlapping contiguous fragments with SepMan (DNASTAR software package). The protein-coding gene and rRNAs sequences were predicted using NCBI BLAST (http://blast.ncbi.nlm.nih.gov/Blast.cgi). The tRNAs and potential RNA secondary structures were identified by using tRNAscan-SE 2.0 (Lowe and Chan, 2016). The structure of tRNASer (AGY) was predicted using sequence comparisons with other published grouper mitogenome. We used the mfold web server to predict the structure of OL (the stem and loop structure) (Zuker, 2003). The EMET mitogenome map was drawn with OGDRAW (http://ogdraw.mpimp-golm.mpg.de/). Mitogenomes from 36 Epinephelinae species were used for comparative analysis. The base composition and codon usage patterns were predicted by MEGA 7.0, and trends of the composition of PCGs and rRNAs were measured by the formulas (Perna and Kocher, 1995):
${\rm{AT}}\; {\rm{skew}}=({\rm{A}}-{\rm{T}})/({\rm{A}}+{\rm{T}}),$
${\rm{GC}}\; {\rm{skew}}=({\rm{G}}-{\rm{C}})/({\rm{G}}+{\rm{C}}).$
2.4 Phylogenetic analysis
Phylogenetic relationships of EMET and other Epinephelinae species were analyzed using data from 35 fish species, including 3 hybrids grouper. Thirteen mitogenomic PCG sequence data were analyzed with Maximum Likelihood (ML) and Neighbor-Joining (NJ) methods (Table 2). The nucleotide sequences of 13 PCGs were aligned with MEGA 7.0 by default settings. The best partitioning scheme and nucleotide substitution models were GTR+I+G selected by PartitionFinder 1.1.1 (Lanfear et al., 2012), and node support was calculated with 1 000 bootstrap replicates.
3 Results
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3.1 Genome structure and organization
The complete mitogenome of EMET was 16 695 bp in length (GenBank accession No. MH748091), containing the typical 37 genes: 13 PCGs, 22 tRNAs, 2 ribosomal RNAs (12S rRNA and 16S rRNA), a control region (D-loop) in 997 bp length and a 36 bp initiation site for transcription and replication (Fig. 2). Of the 37 genes, 28 genes (12 PCGs, 14 tRNA genes, 2 rRNA genes) were encoded on the heavy (H)-strand, and the remaining 9 genes (1 PCGs, 8 tRNA) were encoded on the light (L)-strand (Table 3).
The lengths of the Epinephelinae mitogenome range from 16 418 bp in E. coioides to 17 227 bp in E. bleekeri, with average length of 16 688 bp (Table 4). The EMET mitogenome was longer than the average length in Epinephelinae. The nucleotide base composition of the EMET mitogenome was 28.6%, 28.9%, 16.1% and 26.4% for A, C, G and T, respectively. The calculated A+T content of the complete genome, PCGs, srRNA, lrRNA and the control region was 55.0%, 54.3%, 51.1%, 53.7%, and 66.9%, which were slightly lower compared to the other Epinephelinae species (Table 4). The EMET mitogenome had differences in base preference, and the value of the AT-skew and GC-skew were 0.04, –0.28, respectively. This illustrates that the EMET mitogenome had a bias to A and C.
3.2 Protein-coding genes
In the complete EMET mitogenome, 13 PCGs were encoded from 11 428 bp, accounting for 68.45% of all bases in the mitogenome. The order and location of PCGs were consistent with other vertebrate fish (Table 3). Twelve of the 13 PCGs were encoded on the H-strand, including ND1, ND2, COXI, COXII, ATP8, ATP6, COXIII, ND3, ND4L, ND4, ND5 and Cytb, and ND6 was encoded on the L-strand.
For translation initiation sites, 9 PCGs had ATG, while COXI and ND4 had GTG, ATP6 had CTG, and ND3 had ATA, and all of these patterns were shared by other vertebrates. Translation termination sites included TAA for 7 of the 13 PCGs, COXIII used TA, and the remaining PCGs (ND2, COXII, ND3, ND4, Cytb) used T as their termination codon.
In the complete EMET mitogenome, base content proportion order was as follows: C (28.87%)>A (28.58%)>T (26.46%)>G (16.09%). The utilization rate of G was the lowest, and the A+T was slighter higher than G+C. This pattern is commonly found in PCGs, except for ND4L. In addition, the base composition of the 13 PCGs were different depending on the gene, where the A+T content was highest in Cytb (64.51%), and second highest in COXII (56.73%). Interestingly, the PCGs had a high GC preference, where the GC-skew was 0.28 (Table 5).
The base composition of the coding chain leads to the preference of codon usage. By analyzing the usage of Relative Synonymous Codon Usages (RSCU) (Table 6), we found that C and T were the 2 most frequently used nucleotides, Leu, Ala, Thr, Ile were the 4 most frequently used amino acids, CUC (Leu), CUA (Leu), GCC (Ala) and AUU (Ile) were the 4 most frequently used codons, accounting for 17.07% of all codons in the mitogenome.
3.3 tRNA and rRNA genes
The 22 typical transfer RNA genes ranged from 67 bp in tRNACys to 76 bp in tRNALeu (UUR), and were interspersed across the mitogenome. Of the 22 tRNA genes, 21 were predicted to fold into the typical cloverleaf secondary structures. However, tRNASer (AGY) lacked the DHU loop and was predicted using comparative genomics (Fig. 3). Among tRNAs, eight were encoded on the L-strand, and the rest of were encoded on the H-strand. The small subunit of 12S rRNA gene was 953 bp in length, and was located between tRNAPhe and tRNAVal. The length and position of the 12S rRNA were consistent with the common vertebrate arrangement. The large subunit of the 16S rRNA gene was 1 706 bp in length and was located between tRNAVal and tRNALeu (UUR), similar to other vertebrates. We found that the lengths of 12S rRNA ranged from 940 bp to 961 bp, and the lengths of 16S rRNA ranged from 1673 bp to 1840 bp in Epinephelinae species (Table 4).
3.4 Intergenic spacers and overlapping regions of the mitogenome
The complete mitogenome contains 9 intergenic spacers that vary from 1 bp to 8 bp, which were 33 bp in total. The largest intergenic spacer was 8 bp (AACCGTCA), and was inserted between tRNAAsp and COXII. The second largest was 7 bp, including 2 fragments (AAACATA, CCTATCA), and were inserted between tRNASer (AGY) and tRNALeu (CUN), and between tRNAGlu and Cytb, respectively. The remaining spacers were shorter than 4 bp. In addition, a total of 23 bp short overlaps, ranging from 1 bp to 10 bp, were observed in 5 gene junctions. The biggest overlapping sequence was 10 bp (CTGAGTGTAA), which was located between ATP8 and ATP6. The second was 7 bp, and was located between ND4L and ND4.
3.5 Replication origin of L-strand and control region
In the EMET mitogenome, there were 2 fragment sequences or non-coding regions, including the replication origin of L-strand and the control region. The L-strand replication sequence was 36 bp, and was between tRNAAsn and tRNACys. It was located in a typical cluster of 5 tRNA genes known as the WANCY region. This sequence was predicted to fold into a hairpin structure, consisting of a 28 bp stem and 8 bp loop (Fig. 4), forming a signal to initiate the replication of the L-strand.
The control region was 997 bp long, and was between tRNAPro and tRNAPhe. The AT content of the control region was 66.9%, which was little lower than the average (67.5%), falling between 61.1% in Variola albimarginata and 71.0% in E. fasciatomaculosus (Table 4). The grouper control region consists of several terminaiton-associated sequences (TAS) comprising the extended termination-associated sequences (ETAS) region. In addition, the control region of the E. moara (♀)×E. lanceolatus (♂) mitogenome has 170 bases more than that of E. moara (♀)×E. tukula (♂), and the 170 base sequence contains 10 repeatitive elements and the repeat unit is 17 bases (TATTACATATATGCTGA).
3.6 Maternal inheritance
Comparisons of the mitogenome between the hybrid EMET and its parents E. moara (♀) and E. tukula (♂) were conducted. EMET’s mitogenome was 16 695 bp in length, whereas E. moara and E. tukula were 16 696 bp and 16 503 bp, respectively (Table 4). The mitogenome of EMET shared 99% sequence identify with E. moara, and 91% sequence identify with E. tukula. The PCGs of the mitogenome of the hybrid, E. moara and E. tukula shared the same length (11 428 bp). The main difference of mitogenome in length among the hybrid, E. moara and E. tukula were the length of control region. Compared with E. moara, EMET had lost 1 base, and had a 28 base substitution. All base substitution were purines replaced by the other purine (A/G), or pyrimidine replaced by the other pyrimidine (C/T). In addition, of the 28 base substitutions, 19, 6 and 3 were found in PCGs, control regions and tRNA.
3.7 Phylogenetic analysis
To examine the evolutionary relationship of the hydrid EMET to other Epinephelinae species, a phylogenetic analysis was conducted using the nucleotide sequence from the conserved 13 PCGs of 35 Epinephelinae species, including 3 hybrid grouper individuals (Table 2). A similar topology were observed through both ML and NJ methods (Fig. 5), and the approximate values of the nodes were similar. The 36 species from 14 genera were clustered into 6 different groups with high bootstrap resampling support. Interestingly, Group 1 consisted of 24 species, 20 belonging to the genus Epinephlus and 4 belonging to the genus Cromileptes, Anyperodon, Hyporthodus and Triso, and this pattern was not consistent with conventional morphology-based classification of Epinephelinae species. Group 2 contained 2 species from the genus Cephalopholis and 1 from the genus Aethaloperca. Group 3 consisted of 2 species from the genus Variola. Group 4 consisted of 2 species from the genus Plectropomus. Group 5 contained 1 species from the genus Diploprion and 1 from Grammistes. Group 6 contained 2 different species from the genus Hypoplectrus and Macropodus. EMET was sister to E. moara×E. lanceolatus, and then most closely related to E. moara (100% bootstrap value), and these results support that the mitogenome was inherited maternally.
4 Discussion
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The complete mitogenome of 1 hybrid grouper species, E. moara (♀)×E. tukula (♂), was determined in this study. The complete mitogenome of EMET was 16 695 bp in length, containing the typical 37 genes: 13 PCGs, 22 tRNAs, 2 ribosomal RNAs (12S rRNA and 16S rRNA), D-loop and an initiation site for transcription and replication. The gene content and mitogenome structure were conserved and in accordance with other vertebrates (Zhu and Yue, 2008; Zhuang et al., 2013).
By comparing the mitochondrial genomes of 36 fish species, we found that there are some difference among them in length of complete mitogenome. The length of control region in Epinephelinae species ranged from 720 bp in E. coioides and E. malabaricus to 1 217 bp in E. epistictus, intergenic regions and gene overlaps distributed in mitogenome also plays a role in the length difference of the mitogenome. Variations in the length of the control region, the length of intergenic regions and gene overlaps were accountable to this phenomenon (Moritz et al., 1987). The control region also had several conserved structures, such as a repeat array, which is considered to be the putative control region (Moritz et al., 1987). The length of the control region depends on the length and repetition of the basic repeating units of this region. Some studies have concluded that control regions are associated with the sequences that form the stem and loop structure (Stanton et al., 1994). Interestingly, both samples of the EMET and E. moara×E. lanceolatus shared the same female parent, E. moara, there were differences in the control region of EMET, E. moara×E. lanceolatus and E. moara. One explanation about the variation in control region is DNA mismatch due to DNA secondary structure formation during mitochondria DNA replication (Brown et al., 1992; Cheng et al., 2015). The other explanation is slipped strand mispairing, illegitimate elongation and replication based on termination-associated sequence taken place at control region (Ludwig et al., 2000). The further study is needed to fully understand the mechanisms that give rise to this variability.
As is well-known, mitochondria are generally inherited from maternal. However, different degrees of paternal genetic phenomena about mitochondria were found on a few creatures in many studies (Hoarau et al., 2002; Meusel and Moritz, 1993; Zhao et al., 2004), they provides some evidence for recombination in the mitogenome. In addition, mitogenome has both maternal genetic phenomena and special cases of recombination or introgression of paternal inheritance in hybridization of fish (Guo et al., 2004). Due to the existence of mtDNA paternal inheritance, the paternal genetic effects of mtDNA should be considered when conducting such study related to evolution, classification, disease and animal economic traits. In this study, there were 29 differences in the mitogenome of the hybrid and E. moara, and their distribution were scattered, which was the level of intraspecific variation. So it was not caused by the recombination of the paternal parent (Zhou et al., 2012). It was certain that the mitogenome of the hybrid follow strictly the laws of maternal inheritance.
With the application of mitochondrial and nuclear genes in phylogenetic, traditional views of systematics are experiencing challenges (Craig and Hastings, 2007). In our study, we performed ML and NJ analyses using the concatenated nucleotide sequences of the 13 PCGs, both phylogenetic analyses yielded congruent tree topologies with strong support on all nodes of concern. The trees constructed in this study are quite similar to the one reported by Gao et al. (2017). EMET clusters together with E. moara×E. lanceolatus, E. moara, and they together with other Epinephelus. The genus Variola, Plectropomus, Cephalopholis and Epinephelus are independent of each other, indicating that the molecular phylogeny is in good consistent with the traditionl systermatics. There are, of course, examples of inconsistencies. Four species Anyperodon leucogrammicus, Cromileptes altivelis, Hyporthodus octofasciatus, and Triso dermopterus were a cluster with the species from the Epinephelus. These data may indicate that these 4 species should be classified into the genus Epinephelus, and similar evidence have been supported by other studies (Craig et al., 2001; Ding et al., 2006; Zhu and Yue, 2008). Although some monotypic species have their unique morphological features, the taxonomic revision to synonymize Aethaloperca within genus Cephalopholis, and Grammistes within genus Diploprion (Craig and Hastings, 2007; Gao et al., 2017), and this is corroborated by our phylogenetic analyses. We found that Macropodus opercularis has closed relationships with Hypoplectrus gemma, which suggests they diverged relatively later. In addition, mitogenome exhibits limitations in resolving complicated phylogenetic relationships in many fish lineages (Stepien and Kocher, 1997). So, more genetic data are necessary to fully elucidate the phylogenetic relationships among Epinephelinae fishes.
5 Conclusion
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In this study, the complete mitogenome of the hybrid E. moara (♀)×E. tukula (♂) was 16 695 bp in length, which contained 13 PCGs, 2 rRNA genes, 22 tRNA genes, a replication origin and a control region, which was reported the first time. Phylogenetic analysis based on the sequence of 13 PCGs of 36 species by using ML and NJ methods, which indicated that the mitogenome was inherited maternally in the hybrid individuals, and there were some differences between molecular phylogeny and traditionl systermatics. Thus, more mitogenome and further analyses are in urgent need to elaborate the phylogenetic relationship of Epinephelinae fishes.
Funding
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  • The Key Research and Development Program of Shandong Province under contact No. 2019GHY112063; the Breeding Project of Shandong Province under contract No. 2019LZGC020; the Central Public-interest Scientific Institution Basal Research Fund Chinese Academy of Fishery Sciences under contract Nos 2020XT0601, 2020TD19 and 2020TD25; the Yellow Sea Fisheries Research Institute Research Fees under contract Nos 20603022019002 and 20603022020015.
References
Less
Anderson S, Bankier A T, Barrell B G, et al. 1981. Sequence and organization of the human mitochondrial genome. Nature, 290(5806): 457–465, doi: 10.1038/290457a0
Avise J C. 2009. Phylogeography: retrospect and prospect. Journal of Biogeography, 36(1): 3–15, doi: 10.1111/j.1365-2699.2008.02032.x
Ballard J W O, Whitlock M C. 2004. The incomplete natural history of mitochondria. Molecular Ecology, 13(4): 729–744, doi: 10.1046/j.1365-294X.2003.02063.x
Bibb M J, van Etten R A, Wright C T, et al. 1981. Sequence and gene organization of mouse mitochondrial DNA. Cell, 26(2): 167–180, doi: 10.1016/0092-8674(81)90300-7
Boore J L. 1999. Animal mitochondrial genomes. Nucleic Acids Research, 27(8): 1767–1780, doi: 10.1093/nar/27.8.1767
Boore J L, Daehler L L, Brown W M. 1999. Complete sequence, gene arrangement, and genetic code of mitochondrial DNA of the Cephalochordate Branchiostoma floridae (Amphioxus). Molecular Biology and Evolution, 16(3): 410–418, doi: 10.1093/oxfordjournals.molbev.a026122
Brown J R, Beckenbach A T, Smith M J. 1992. Mitochondrial DNA length variation and heteroplasmy in populations of white sturgeon (Acipenser transmontanus). Genetics, 132(1): 221–228
Brown W M, George Jr M, Wilson A C. 1979. Rapid evolution of animal mitochondrial DNA. Proceeding of the National Academy of Sciences of the United States of America, 76(4): 1967–1971, doi: 10.1073/pnas.76.4.1967
Chang Y S, Huang F L, Lo T B. 1994. The complete nucleotide sequence and gene organization of carp (Cyprinus carpio) mitochondrial genome. Journal of Molecular Evolution, 38(2): 138–155, doi: 10.1007/BF00166161
Cheng S S, Senoo S, Siddiquee S, et al. 2015. Genetic variation in the mitochondrial genome of the giant grouper Epinephelus lanceolatus (Bloch, 1790) and its application for the identification of broodstock. Aquaculture Reports, 2: 139–143, doi: 10.1016/j.aqrep.2015.09.003
Craig M T, Hastings P A. 2007. A molecular phylogeny of the groupers of the subfamily Epinephelinae (Serranidae) with a revised classification of the Epinephelini. Ichthyological Research, 54(1): 1–17, doi: 10.1007/s10228-006-0367-x
Craig M T, Pondella II D J, Franck J P C, et al. 2001. On the status of the serranid fish genus Epinephelus: evidence for paraphyly based upon 16S rDNA sequence. Molecular Phylogenetics and Evolution, 19(1): 121–130, doi: 10.1006/mpev.2000.0913
DeMarais B D, Dowling T E, Douglas M E, et al. 1992. Origin of Gila seminuda (Teleostei: Cyprinidae) through introgressive hybridization: Implications for evolution and conservation. Proceedings of the National Academy of Sciences of the United States of America, 89(7): 2747–2751, doi: 10.1073/pnas.89.7.2747
Ding Shaoxiong, Zhang Xuan, Guo Feng, et al. 2006. Molecular phylogenetic relationships of China Sea groupers based on cytochrome b gene fragment sequences. Science in China: Series C Life Sciences, 49(3): 235–242, doi: 10.1007/s11427-006-0235-y
Gao Fengtao, Wei Min, Zhu Ying, et al. 2017. Characterization of the complete mitochondrial genome of the hybrid Epinephelus moara ♀×Epinephelus lanceolatus♂, and phylogenetic analysis in subfamily epinephelinae. Journal of Ocean University of China, 16(3): 555–563, doi: 10.1007/s11802-017-3202-2
Glamuzina B, Glavić N, Skaramuca B, et al. 2001. Early development of the hybrid Epinephelus costae ♀×E. marginatus ♂. Aquaculture, 198(1–2): 55–61
Guo Xinhong, Liu Shaojun, Zhang Chun, et al. 2004. Comparative and evolutionary analysis of the cytochrome b sequences in cyprinids with different ploidy levels derived from crosses. Genetica, 121(3): 295–301, doi: 10.1023/B:GENE.0000039847.82917.c4
Heemstra P C, Randall J E. 1993. Groupers of the World (Family Serranidae, subfamily Epinephelinae): An Annotated and Illustrated Catalogue of the Grouper, Rockcod, Hind, Coral Grouper and Lyretail Species Known to Date. Rome: Food and Agriculture Organization of the United Nations, 1–10
Hoarau G, Holla S, Lescasse R, et al. 2002. Heteroplasmy and evidence for recombination in the mitochondrial control region of the flatfish Platichthys flesus. Molecular Biology and Evolution, 19(12): 2261–2264, doi: 10.1093/oxfordjournals.molbev.a004049
James C M, Al-Thobaiti S A, Rasem B M, et al. 1999. Potential of grouper hybrid (Epinephelus fuscoguttatus×E. polyphekadion) for aquaculture. Naga, The World Fish Center, 22(1): 19–23
Lanfear R, Calcott B, Ho S Y W, et al. 2012. Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29(6): 1695–1701, doi: 10.1093/molbev/mss020
Liu Lili, Xie Hongbing, Yu Qifang, et al. 2016. Determination and analysis of the complete mitochondrial genome sequence of taoyuan chicken. Mitochondrial DNA Part A, 27(1): 371–372, doi: 10.3109/19401736.2014.895991
Liu M, Li J L, Ding S X, et al. 2013. Epinephelus moara: a valid species of the family Epinephelidae (Pisces: Perciformes). Journal of Fish Biology, 82(5): 1684–1699, doi: 10.1111/jfb.12112
Lowe T M, Chan P P. 2016. tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Research, 44(W1): W54–W57, doi: 10.1093/nar/gkw413
Ludwig A, May B, Debus L, et al. 2000. Heteroplasmy in the mtDNA control region of sturgeon (Acipenser, Huso and Scaphirhynchus). Genetics, 156(4): 1933–1947
Meusel M S, Moritz R F A. 1993. Transfer of paternal mitochondrial DNA during fertilization of honeybee (Apis Mellifera L.) eggs. Current Genetics, 24(6): 539–543, doi: 10.1007/BF00351719
Moritz C, Dowling T E, Brown W M. 1987. Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annual Review of Ecology and Systematics, 18: 269–292, doi: 10.1146/annurev.es.18.110187.001413
Oh B S, Oh D J, Jung M M, et al. 2012. Complete mitochondrial genome of the longtooth grouper Epinephelus bruneus (perciformes, serranidae). Mitochondrial DNA, 23(2): 137–138, doi: 10.3109/19401736.2012.660928
Peng Rui, Zeng Bo, Meng Xiuxiang, et al. 2007. The complete mitochondrial genome and phylogenetic analysis of the giant panda (Ailuropoda melanoleuca). Gene, 397(1–2): 76–83, doi: 10.1016/j.gene.2007.04.009
Perna N T, Kocher T D. 1995. Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal of Molecular Evolution, 41(3): 353–358, doi: 10.1007/BF01215182
Qu Meng, Zhang Xiang, Ding Shaoxiong. 2012. Complete mitochondrial genome of yellow grouper Epinephelus awoara (Perciformes, Epinephelidae). Mitochondrial DNA, 23(6): 432–434, doi: 10.3109/19401736.2012.710217
Stanton D J, Daehler L L, Moritz C C, et al. 1994. Sequences with the potential to form stem-and-loop structures are associated with coding-region duplications in animal mitochondrial DNA. Genetics, 137(1): 233–241
Stemshorn K C, Reed F A, Nolte A W, et al. 2011. Rapid formation of distinct hybrid lineages after secondary contact of two fish species (Cottus sp.). Molecular Ecology, 20(7): 1475–1491, doi: 10.1111/j.1365-294X.2010.04997.x
Stepien C A, Kocher T D. 1997. Molecules and morphology in studies of fish evolution. In: Kocher T D, Stepien C A, eds. Molecular Systematics of Fishes. Amsterdam: Elsevier, 1–11
Tian Yongsheng, Tang Jing, Ma Wenhui, et al. 2019. Development and growth of hybrid offspring of brown grouper Epinephelus fuscoguttatus (♀) × blue speckled grouper Epinephelus tulcula (♂) using cryopreserved sperm. Progress in Fishery Sciences (in Chinese), 40(6): 36–47
Wang Yuguo. 2017. Natural hybridization and speciation. Biodiversity Science (in Chinese), 25(6): 565–576, doi: 10.17520/biods.2017041
Zhao X, Li N, Guo W, et al. 2004. Further evidence for paternal inheritance of mitochondrial DNA in the sheep (Ovis aries). Heredity, 93(4): 399–403, doi: 10.1038/sj.hdy.6800516
Zhou Hanlin, Yang Sen, Gao Chuan, et al. 2012. Analysis of genetic variability of mtDNA COI genes between two grouper hybrids and their parents. Journal of Tropical Organisms (in Chinese), 3(1): 1–10
Zhu Kecheng, Huang Guiju, Zhang Dongling, et al. 2016. The complete nucleotide sequence of malabar grouper (Epinephelus malabaricus) mitochondrial genome. DNA Sequence, 27(3): 2087–2088
Zhu Zeyuan, Yue Genhua. 2008. The complete mitochondrial genome of red grouper Plectropomus leopardus and its applications in identification of grouper species. Aquaculture, 276(1–4): 44–49, doi: 10.1016/j.aquaculture.2008.02.008
Zhuang Xuan, Ding Shaoxiong, Wang Jun, et al. 2010. A set of 16 consensus primer pairs amplifying the complete mitochondrial genomes of orange-spotted grouper (Epinephelus coioides) and Hong Kong grouper (Epinephelus akaara). Molecular Ecology Resources, 9(6): 1551–1553
Zhuang Xuan, Qu Meng, Zhang Xiang, et al. 2013. A comprehensive description and evolutionary analysis of 22 grouper (Perciformes, Epinephelidae) mitochondrial genomes with emphasis on two novel genome organizations. PLoS One, 8(8): e73561, doi: 10.1371/journal.pone.0073561
Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research, 31(13): 3406–3415, doi: 10.1093/nar/gkg595
Appendix
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Year 2020 volume 39 Issue 12
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Article Info
doi: 10.1007/s13131-020-1689-7
  • Receive Date：2019-07-11
  • Online Date：2026-03-31
  • Published：2020-12-25
Article Data
Affiliations
History
  • Received：2019-07-11
  • Accepted：2020-04-27
Funding
The Key Research and Development Program of Shandong Province under contact No. 2019GHY112063; the Breeding Project of Shandong Province under contract No. 2019LZGC020; the Central Public-interest Scientific Institution Basal Research Fund Chinese Academy of Fishery Sciences under contract Nos 2020XT0601, 2020TD19 and 2020TD25; the Yellow Sea Fisheries Research Institute Research Fees under contract Nos 20603022019002 and 20603022020015.
Affiliations
    1 College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China
    2 Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266071, China
    3 Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
    4 College of Fisheries and Life Science, Dalian Ocean University, Dalian 116023, China
    5 Laizhou Mingbo Aquatic Co. Ltd., Laizhou 261400, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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