Comparative mitochondrial genome analysis of Cynoglossidae (Teleost: Pleuronectiformes) and phylogenetic implications

Comparative mitochondrial genome analysis of Cynoglossidae (Teleost: Pleuronectiformes) and phylogenetic implications

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Bilin Hu¹^,², Tingqi Jiang¹^,², Liming Wei¹^,², Nannan Zhang¹^,², Kaixin Wang¹^,², Liqin Liu¹^,², Bingjian Liu¹^,², Jing Liu¹^,², Zhenming Lü¹^,², Li Gong¹^,²^,^*

Acta Oceanologica Sinica | 2023, 42(11) : 69 - 80

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Acta Oceanologica Sinica | 2023, 42(11): 69-80

• Marine Biology •

Comparative mitochondrial genome analysis of Cynoglossidae (Teleost: Pleuronectiformes) and phylogenetic implications

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Bilin Hu¹^,², Tingqi Jiang¹^,², Liming Wei¹^,², Nannan Zhang¹^,², Kaixin Wang¹^,², Liqin Liu¹^,², Bingjian Liu¹^,², Jing Liu¹^,², Zhenming Lü¹^,², Li Gong¹^,²^,^*

Affiliations

¹ National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, Zhoushan 316022, China

² Marine Science and Technology College, Zhejiang Ocean University, Zhoushan 316022, China

Published: 2023-11-25 doi: 10.1007/s13131-023-2189-3

Outline

Abstract

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Generally, a teleostean group (e.g., family or genus) owns one type or a set of similar mitochondrial gene arrangement. It is interesting, however, that four different types of gene arrangement have been found in the mitochondrial genome (mitogenome) of Cynoglossidae species. So far, the possible mechanisms of mitogenomic gene rearrangement and its potential implications have aroused widespread attention and caused lots of controversy. Here, a total of 21 Cynoglossidae mitogenomes and a newly sequenced mitogenome of Cynoglossus puncticpes (Pleuronectiformes: Cynoglossidae) were compared. The length ranges from 16 417 bp to 18 369 bp, which is mainly caused by the length heteroplasmy of control region (CR). Further analysis reveals that the difference of tandem repeats acts as a determining factor resulting in the length heterogeneity. Like most gene rearrangements of Cynoglossinae mitogenomes, tRNA-Gln gene encoded by the L-strand has translocated to the H-strand (Q inversion), accompanied by the translocation of CR in C. puncticpes mitogenome. The typical IQM order (tRNA-Ile-Gln-Met) changed to QIM order. Tandem duplication/random loss and mitochondrial recombination were accepted as the most possible models to account for the rearrangements in C. puncticpes mitogenome. Phylogenetic trees showed a strong correlation between the gap spacer in the rearranged QIM area and phylogeny, which provides a fresh idea for phylogenetic studies in future.

Key words

mitogenome / gene rearrangement / tandem duplication/random loss / mitochondrial inversion / control region / phylogenetic study

Cite this Article

Bilin Hu, Tingqi Jiang, Liming Wei, Nannan Zhang, Kaixin Wang, Liqin Liu, Bingjian Liu, Jing Liu, Zhenming Lü, Li Gong. Comparative mitochondrial genome analysis of Cynoglossidae (Teleost: Pleuronectiformes) and phylogenetic implications[J]. Acta Oceanologica Sinica, 2023 , 42 (11) : 69 -80 . DOI: 10.1007/s13131-023-2189-3

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1 Introduction

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The vertebrate mitochondrial genome (mitogenome) is typically a double-stranded circular DNA molecule, with a size of 14–22 kb. It contains 13 protein-coding genes (PCGs), 22 transfer RNA genes (tRNAs), two ribosomal RNA genes (12S and 16S), an L-strand replication origin (O_L) and a putative control region (CR) (Boore, 1999). Generally, gene numbers and their arrangements in the mitogenome are considered highly conserved. But with the growing number of mitogenomes in recent decades, increasing gene rearrangements have been observed in various vertebrate mitogenomes, such as amphibians, reptiles and fish (Zhang et al., 2018; Yan et al., 2008; Lü et al., 2019). Gong et al. estimated the rearrangement rate was about 4% in fish mitogenomes, mainly existing in Anguilliformes, Myctophiformes, Lophiiformes and Pleuronectiformes mitogenomes (Gong et al., 2013a).

There are three main rearrangement types in vertebrate mitogenomes, including shuffling, translocation and inversion. A single rearrangement type or multiple rearrangement events may occur in mitogenomes. So far, four main mechanisms have been proposed to account for mitogenomic rearrangements, including tandem duplication/random loss (TDRL) model (Moritz and Brown, 1987), intra-mitochondrial recombination model (Poulton et al., 1993), tRNA mis-priming model (Cantatore et al., 1987) and tandem duplication/non-random loss (TDNL) model (Lavrov et al., 2002). TDRL and intra-mitochondrial recombination are two most accepted models. The former has been widely used to explain the translocation of genes encoded on the same strand (Lü et al., 2019; Zhang et al., 2022a), and the latter is commonly used to account for inversion event occurring between different strands (from light strand to heavy strand, and vice versa) (Kong et al., 2009; Gong et al., 2019a).

Tongue soles (Pleuronectiformes: Cynoglossidae), the most recently diverged taxa of flatfish, derived large numbers of morphologically similar species. According to morphological taxonomy, Cynoglossidae is divided into two subfamilies, Symphurinae and Cynoglossinae. Due to their special morphological characteristics, the classification of tongue soles (especially the Cynoglossinae) has long been a controversial issue (Li and Wang, 1995; Menon, 1977; Chapleau, 1988). For example, early taxonomists divided the speciose Cynoglossinae into two genera (Paraplagusia and Cynoglossus) mainly based on the characters of fringes on the lips and the number of lateral lines on the ocular side. While some researchers suggested divide the original genus Cynoglossus into seven new genera mainly based on the number of lateral line and left nostril. Although Li and Wang (1995) supported the similar taxonomic characters, they reduced these seven genera to the level of subgenera. Menon (1977) divided Cynoglossus into six groups mainly based on the number of scales between the lateral lines, type of scales, location of mouth and number of caudal fins. However, there was no detailed description about the classification of Cynoglossus in Nelson et al. (2016) taxonomy system. Recently, plenty of molecular evidence supported the non-monophyly of Cynoglossus (Mu et al., 2015; Gong et al., 2020; Wang et al., 2020a), raising doubts about the rationality of this genus. Unfortunately, there is still a lack of comprehensive and systematic study of these controversial taxa.

Generally, a teleostean group (e.g., family or genus) possesses only one type or a set of similar mitochondrial gene arrangement (Miya et al., 2003; Luo et al., 2019). Taking Pleuronectiformes for example, which possess the most diversified gene rearrangement patterns in teleost mitogenomes, Bothidae, Samaridae, Citharidae and Poecilopsettidae exclusively own its unique rearrangement representing the corresponding families (Luo et al., 2019; Shi et al., 2013, 2014a). Interestingly, there have been four different types of rearrangement found in Cynoglossidae mitogenomes, including one typical arrangement type (no rearrangement) and three rearrangement types (Shi et al., 2015a; Gong et al., 2020; Kong et al., 2009). Symphurus plagiusa (Cynoglossidae: Symphurinae) shares the typical arrangement type with most vertebrate mitogenomes, while its close relative, S. orientalis captures a diverse rearrangement type (Shi et al., 2015a). Cynoglossinae mitogenomes shared other two rearrangement types, both of which were featured by the translocation of CR and inversion of tRNA-Q gene. The main difference between these two types of mitogenomes lies in the IQM cluster (tRNA-Ile-Gln-Met) order. Most of the Cynoglossinae mitogenomes are presented by QIM order, while 3 Cynoglossinae mitogenomes (Cynoglossus melampetalus, C. interruptus and C. robustus) are featured by IMQ order (Kong et al., 2009; Gong et al., 2020).

Accordingly, the complete mitogenome sequence of C. puncticpes (Cynoglossidae: Cynoglossinae) was newly determined and annotated in this study. Combined with other 21 published Cynoglossidae mitogenomes, the mitogenome composition, control region structure, rearrangement types, possible rearrangement processes and interpretations were comparatively analyzed. Also, the relationship between mitogenomic rearrangement and phylogeny of Cynoglossidae were explored. These results will contribute to better understanding the characteristics of flatfish mitogenomes, rearrangement mechanisms and its potential application in phylogenetic studies.

2 Materials and methods

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2.1 Sample collection and genome survey sequencing

Specimens were collected from Zhuhai, Guangdong, China, (22^◦00′15′′N, 113^◦18′17′′E). Muscle tissue was stored in 95% ethanol at –80℃. Total genomic DNA was extracted using a standard phenol-chloroform method for muscle tissue. DNA was treated with RNase A to produce pure, RNA-free DNA. Two paired-end DNA libraries were constructed with insert size of 350 bp, and then sequenced using the Illumina HiSeq4000 platform following the manufacturer’s protocol. The library construction and sequencing were performed at Onemore Technology Company (Wuhan, China).

2.2 K-mer analysis and mitochondrial genome assembly

After removing low quality reads, all clean data were used to perform K-mer analysis using software GCE v1.0.0 (Liu et al., 2013). Based on the results of the K-mer analysis, information on peak depth and the number of predicted best K-mer were obtained and used to estimate the size of the genome. Its relationship was expressed by using the following algorithm: Genome size = kmer_num/peak_depth, where K-mer_num indicates the total number of predicted best K-mer, and peak_depth indicates the expected value of the K-mer depth. Also, the heterozygosity ratio and repeat sequence ratio were estimated based on the K-mer analysis. Subsequently, the filtered clean data were assembled and mapped to complete mitogenome sequence using NOVOPlasty v4.3.1 (Dierckxsens et al., 2017).

2.3 Mitogenome annotation and sequence analysis

The newly complete mitogenome of C. puncticeps was annotated using the software of Sequin (version 15.10, http://www.ncbi.nlm.nih.gov/Sequin/). The PCGs were determined by their open reading frame following the vertebrate mtDNA translation table. The predicted boundaries of ribosomal RNA genes were determined using NCBI-BLAST (http://blast.ncbi.nlm.nih.gov). Transfer RNA genes were determined the location and the secondary structure predicted by the MITOS Web Server and tRNA scan-SE 1.21. CR was determined by the locations of adjacent genes. Tandem repeat units of the CR were identified with Tandem Repeats Finder 4.09. The base composition, sequence similarity and genetic distance were analyzed with MEGA X. The strand asymmetry was calculated using the following formulas: AT-skew = (A − T)/(A + T); GC-skew = (G − C)/(G + C). Genome sequence similarity of the C. puncticeps mitogenome with other Cynoglossidae mitogenomes was performed using the CG View Comparison Tool (CCT). CCT uses BLAST to compare a query genome with all other genomes and then presents the results as a circular map.

2.4 Phylogenetic analysis

A total of 22 Cynoglossidae mitogenomes were used to reconstruct the phylogenetic relationships, including 21 mitogenomes downloaded from the GenBank database and one newly determined sequence in this study (C. puncticeps). Soleidae species have been thought to be most closely related to Cynoglossidae; therefore, two Soleidae species, Zebrias zebrinus and Z. crossolepis, were selected as the outgroup. Fasta files with the nucleotide sequences for all 13 PCGs were extracted from the GenBank files using PhyloSuite (Zhang et al., 2020). Sequences were aligned using Clustal X 2.0 (Larkin et al., 2007) with the default parameters and manually checked with BioEdit (Hall, 1999). The ambiguous sequences were eliminated using Gblocks (Talavera and Castresana, 2007). Subsequently, the sequences were concatenated into a single alignment and converted into input files (Phylip and Nexus format) for phylogenetic analyses. Both maximum likelihood (ML) and Bayesian inference (BI) were employed for phylogenetic analyses. ML analysis was conducted using IQ-TREE (Nguyen et al., 2015), under an ML + rapid bootstrap (BS) algorithm with 1000 replicates. The BI analysis was carried out in MrBayes 3.2.6 (Ronquist et al., 2012) with default parameters. Two independent runs of four Markov chain Monte Carlo (MCMC) chains (one cold chain and three hot chains) were simultaneously run for 3 × 10⁶ generations, with sampling conducted every 1 000 generations and the first 25% of the generations were discarded as burn-in. To guarantee the stationarity had been reached, the average standard deviation of split frequencies was set below 0.01. (Katoh et al., 2002; Lanfear et al., 2017)

3 Results and discussion

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3.1 Genome structure, composition and skewness

The complete mitogenome of C. puncticeps (GenBank accession number OP_573760) is a closed-circular molecule of 17 158 bp in length. The gene content is typical with other teleostean mitogenomes, including 13 PCGs, 22 tRNA genes, 2 rRNA genes and a putative CR. Except ND6 and seven tRNAs (tRNA-Pro, Ala, Asn, Cys, Tyr, Ser₁, Glu), which are distributed on the light (L-) strand, the remaining genes are distributed on the heavy (H-) strand (Fig. 1, Table 1).

In this study, the sequence features of the newly determined C. puncticeps mitogenome and other 21 Cynoglossidae mitogenomes were compared. The mitogenomes have obvious variation in size, ranging from 16417 bp (C. abbreviates) to 18369 bp (C. trigrammus). All mitogenomes are rich in As and Ts, with the A+T content ranging from 53.8% (Symphurus plagiusa) to 62.0% (C. puncriceps). AT-skew and GC-skew of all mitogenomes are shown in Table 1, which are consistent with most metazoan mitogenomes (positive AT-skew and negative GC-skew) (Gong et al., 2019b; Zhang et al., 2021; Miya et al., 2003). Using C. puncticeps mitogenome as the reference sequence, all Cynoglossidae mitogenomes were compared using CCT. Obviously, the inner most two circles (S. orientails and S. plagiusa mitogenomes) show great difference between other 20 circles in most regions due to their divergent gene arrangements (Fig. 1). Overall, all Cynoglossinae mitogenomes are observed to be conserved, except the similarity of the entire control region, 3' end of ND2 and ND5, and 5' end of ND6 (Fig. 1).

3.2 PCGs and codon usage

The start/stop codons of 22 Cynoglossidae mitogenomes were compared. The results reveal that there are five start codons (ATG, ATT, ATA, ATC and GTG), three complete stop codons (TAA, TAG and AGA) and two incomplete termination codons (TA and T). ATG and GTG are two most frequently used start codons almost occurring in all PCGs, and an unusual start codon (ATC) is found exclusively in C. melampetalus mitogenome (ND3) (Table 2).

Due to base-composition asymmetry of the mitogenomes, value of GC-skew can act as a signal of the origin and end point of the leading strand, and the transformation from leading strand to lagging strand during DNA replication. Hence, the coding strand of certain gene can be confirmed by the value of GC-skew. Generally, positive GC-skew value indicates the gene is encoded by the H-strand; whereas, negative GC-skew value indicates the L-strand. In this study, the value of GC-skew of 13 PCGs of 22 Cynoglossidae mitogenomes was calculated. The result shows that except for ND6 gene has a positive GC-skew value, the remaining 12 PCGs have a negative GC-skew value, suggesting the ND6 gene is encoded by L-strand, and the remaining 12 PCGs are encoded by H-strand (Fig. 2).

The mitochondrial COI gene has long been acted as a DNA barcoding for species identification. To investigate possible synonyms in these Cynoglossidae species, genetic distance and sequence similarity of COI gene among 22 Cynoglossidae mitogenomes were calculated. The maximum genetic distance value is 0.732 (between S. orientalis and C. zanzibarensis), and the corresponding sequence similarity has a lowest value (71.5%). The minimum genetic distance value is 0.002 (between C. interruptus and C. robustus), and their sequence similarity reaches up to 99.8%, suggesting that they might be the same species. The overall sequence similarity of the complete mitogenomes (96.5%) and the phylogenetic relationship of these two species also support this point (Table 3).

3.3 Control region

CR is the most variable region in mitogenomes because of its fast evolution rate compared with other genes. It is typically located between tRNA-Pro and tRNA-Phe genes, with an extremely high AT content and abundant tandem repeat units, performing an important function in replication and transcription. However, the CR of all 20 Cynoglossinae mitogenomes have translocated downstream to the 3' end of ND1 gene (Fig. 3). In order to better understand the variations of CR, 22 Cynoglossidae CRs were compared. The result reveals a high AT content, ranging from 64.1% (C. zanzibarensis)−70.6% (S. orientalis). The length also has a significant variation ranging from 655 bp (C. bilineatus) to 1433 bp (C. puncticeps), which is the main contributor for length heteroplasmy of the complete mitogenomes of Cynoglossidae species. Further analysis shows that the difference of tandem repeats acts as a determining factor resulting in the length heterogeneity. Except C. senegalensis and C. sinicus, the remaining 20 CRs possess diverse tandem repeats differing in motifs and number of copies, which ranges from 8 bp to 73 bp and 1.9 to 40.2 copies, respectively. Although CR in most vertebrate mitogenomes (e.g., amphibians, reptiles, birds, fish and mammals) captures several conserved sequence blocks (White and Martin, 2009; Zhao et al., 2006; Brown et al., 1986; Gong et al., 2015), no obvious conserved sequences were found in Cynoglossidae mitogenomes due to its high variation (Fig. S1).

3.4 Gene rearrangement

Gene order in 22 Cynoglossidae mitogenomes were compared. Except that in S. plagiusa (Symphurinae) mitogenome, the remaining 21 mitogenomes underwent varying degrees of gene rearrangement events compared with that in ancestral vertebrate mitogenomes. Three types of mitogenomic rearrangement were found, represented by (Ⅰ) S. orientalis (Symphurinae) mitogenome (Fig. 4b); (Ⅱ) C. puncticeps and other 16 Cynoglossinae mitogenomes (Fig. 4c); and (Ⅲ) C. melampetalus, C. robustus and C. interruptus (Cynoglossinae) mitogenomes (Fig. 4d).

Gene arrangements in S. orientalis mitogenome is featured by the translocation of tRNA-Val and tRNA-Met genes downstream to the 3' end of the 16S rRNA gene. It is a unique rearrangement phenomenon in Pleuronectiformes mitogenomes and was first reported by Shi et al. (2015a). The authors explained that the double O_L-like structures-initiated DNA synthesis twice during mitochondrial replication, causing tandem duplication of the genes located between the CR and the WANCY region. Generally, mitogenome only maintains one set of functional genes, the duplicated genes would randomly lose their functions and became pseudogenes, shorter non-coding sequences or even be eliminated from the genome (Fig. 4b). Six large intergenic spacers (over 20 bp) in the rearranged regions suggested a duplication and deletion process during mitochondrial replication.

All Cynoglossinae mitogenomes underwent remarkable gene rearrangements. The tRNA-Gln gene encoded by the L-strand has translocated to the H-strand (Q inversion) and the control region translocated downstream to the place between ND1. Interestingly, two types of gene rearrangements coexist in Cynoglossinae mitogenomes. The difference between these two types of mitogenomes lies in the rearrangement of IQM cluster (tRNA-Ile-Gln-Met). Most of the Cynoglossinae mitogenomes (17/20, including C. puncticeps in this study) are presented by QIM order (Fig. 4c), while only 3 Cynoglossinae mitogenomes are featured by IMQ order (Fig. 4d). Kong et al. (2009) reported the first gene rearrangement phenomenon in Cynoglossidae mitogenomes, followed by increasingly uniform patterns. Intra-mitochondrial recombination and tandem duplication/random loss model were widely accepted to explain the rearrangement events (Mu et al., 2015; Wang et al., 2020a; Gong et al., 2013b). In C. puncticeps and other 16 Cynoglossinae mitogenomes, the typical IQM cluster (ancestral teleosts gene order with no rearrangement) underwent an inverted duplication, forming an M’- Q’- I’- I- Q- M dimeric block (the symbol’ indicates inverted gene). In the next step, the redundant genes lost their functions through random deletion, namely M’- Q’- I’- I- Q- M (the symbol indicates the deleted gene). Thus, a new Q’IM gene order was generated (Fig. 4c). Gong et al. (2020) found the first unusual rearrangement in C. melampetalus mitogenome, which was a unique phenomenon in Cynoglossidae mitogenomes. They adopted the same models to account for the distinctive rearrangement. It was speculated that the Q’IM cluster in most Cynoglossinae mitogenomes formed a Q’- I- M- Q’- I- M dimeric block after duplication, then followed by random deletion of the supernumerary genes, Q’- I- M- Q’- I- M. Thus, a new IMQ’ gene order in Cynoglossidae mitogenome emerged (Fig. 4d). Identical gene rearrangements were found in C. robustus and C. interruptus mitogenomes.

3.5 Phylogenetic analysis of Cynoglossidae and non-monophyly of Cynoglossu

In this study, the phylogenetic relationship of Cynoglossidae species was reconstructed based on the nucleotide sequences of 13 PCGs using ML and BI methods. ML tree and BI tree produced an identical topological structure. Here, only one topology (ML) with both support values is displayed (Fig. 5). It is comprised of two clades. Symphurus orientalis and S. plagiusa form the Symphurinae clade, locating in the base of the tree. Three Paraplagusia species (P. bilineata, P. japonica and P. blochii) and 17 Cynoglossus species constitute the Cynoglossinae clade. It is worth noting that three Paraplagusia species cluster into a group, while the other 17 Cynoglossus species form a paraphyletic relationship. Among them, C. monopus and C. puncticeps form a sister clade with three Paraplagusia species, suggesting these two Cynoglossus species have a closer relationship with Paraplagusia than with other Cynoglossus species.

Many studies have contributed to the classification and phylogeny of tongue soles (Cynoglossidae) based on morphological taxonomy (Chapleau, 1988; Menon, 1977). Chapleau (1988) provided the first exhaustive comparative osteological study of Cynoglossidae, and proposed two subfamilies (Symphurinae and Cynoglossinae) of Cynoglossidae. Since then, almost all of the studies followed this classification system. However, increasing number of molecular evidence revealed that Symphurinae were quite different from their closely related species, Cynoglossinae. For example, the mitogenomic rearrangements in these two taxa are strikingly different (Fig. 4). Generally, a teleostean group (belonging to the same order or family) possesses only one type or a set of similar mitochondrial gene arrangement (Zhang et al., 2022b; Luo et al., 2019; Montaña-Lozano et al., 2022). It is a rare phenomenon that two sets of various mitochondrial gene arrangement coexist in a family, especially in teleostean mitogenomes (Lü et al., 2019; Shi et al., 2015a). Besides, the genetic distance and the branch length in the phylogenetic tree also suggest that these two taxa are raised to the rank of family. Of course, an examination of the morphology and molecular data of more species belonging to Symphurinae are needed to further test this proposal.

The speciose Cynoglossinae are divided into two genera (Paraplagusia and Cynoglossus) mainly based on the characters of fringes on the lips (the former possesses fringes on the lips on eyed side; the latter lacks fringes on the lips). Numerous studies showed Parapaglusia was monophyletic, while no evidence was found to support a similar status for Cynoglossus. In fact, growing number of molecular researches including our results corroborate the non-monophyly of Cynoglossus (Mu et al., 2015; Wang et al., 2020a; Gong et al., 2020). With the increasing number of tongue soles, the classification of Cynoglossus has been largely disputed (Li and Wang, 1995; Nelson et al., 2016; Chapleau, 1988; Menon, 1977). Previous researchers suggested divided the original genus Cynoglossus into seven new genera manily based on the number of lateral line and left nostril, including Cynoglossus Hamilton 1822, Arelia Kaup 1858, Trulla Kaup 1858, Icania Kaup 1858, Areliscus Jordan et Snyder 1900, Dollfusichthys Chabanaud 1931 and Cynoglossoides Smith 1953. While Li and Wang (1995) degraded these genera to the rank of subgenus. However, Menon (1977) did not regard lateral line and left nostril as the effective taxonomic characters. Instead, number of scales between the lateral lines, type of scales, location of mouth and number of caudal fins were synthesized to divide Cynoglossus into six groups, including canariensis, kopsii, arel, cynoglossus, carpenter and heterolepis. While there was no detailed description about the classification of Cynoglossus in Nelson et al.’s taxonomy system (Nelson et al., 2016). According to WoRMS database (https://www.marinespecies.org/aphia.php?p=taxdetails&id=126112), the genus Cynoglossus possesses about 112 species. More purposeful research is needed on each of these subgenera or groups with more integrated approaches to clarify the speciose taxa.

3.6 Implications of QIM spacers

The typical IQM order in ancestral vertebrate mitogenomes changed to QIM or IMQ order in all Cynoglossinae mitogenomes. Previous studies suggested that gene rearrangements and length of gap spacer in the rearranged area could reflect the evolutional trace of mitogenomes, and further revealed the phylogenetic relationships (Gong et al., 2020; Zhang et al., 2022b; McKnight and Shaffer, 1997). Here, the length of gap spacer in the rearranged area were compared. In C. puncticeps and other 16 Cynoglossinae mitogenomes, the intergenic space between Q and I (G1) ranged from 3 bp (C. joyneri) to 160 bp (C. zanzibarensis); 5 bp (P. bilineata and P. blochii) to 35 bp (C. gracilis) between I and M (G2). That between M and ND2 (G3) was consistent in all 17 Cynoglossinae species (1 bp). In C. melampetalus, C. interruptus and C. robustus mitogenomes featured with IMQ gene order, large gaps existed between M and Q (186−194 bp), Q and ND2 (77−91 bp), and that between I and M was comparatively small (11−12 bp). Although no obvious correlation was found between G2, G3 and the phylogenetic relationship, the intergenic space between Q and I (G1) had a decreasing trend with the evolution process (excluding the gap spacers in IMQ cluster in C. melampetalus, C. interruptus and C. robustus mitogenomes). In the base of phylogenetic tree (C. zanzibarensis, C. senegalensis, C. sinicus, and C. bilineatus), the intergenic space of G1 showed the largest lengths (121−160 bp). In the middle branches of the tree, the intergenic space reduced to a moderate length range (73−88 bp). Reversely, in the top of the tree, the intergenic space decreased to the smallest gaps (3−19 bp). This trend was in accordance with our previous result (Gong et al., 2020), suggesting intergenic spacer in the rearranged area could reveal the phylogenetic relationships in some certain. However, the position of the two newly sequenced C. nanhaiensis and C. itinus challenged this trend in this study. Accordingly, more taxon samplings and more new molecular markers are needed to uncover the authentic phylogenetic relationships and the potential application prospect of gene rearrangements.

Funding

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The Natural Science Foundation of Zhejiang Province under contract No. LY21C190007; the Basic Scientific Research Operating Expenses of Zhejiang Provincial Universities under contract No. 2021JZ003; the Zhoushan Science and Technology Bureau under contract No. 2021C21007.

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doi: 10.1007/s13131-023-2189-3

Receive Date：2022-12-27
Online Date：2025-11-22
Published：2023-11-25

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Received：2022-12-27
Accepted：2023-02-21

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The Natural Science Foundation of Zhejiang Province under contract No. LY21C190007; the Basic Scientific Research Operating Expenses of Zhejiang Provincial Universities under contract No. 2021JZ003; the Zhoushan Science and Technology Bureau under contract No. 2021C21007.

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¹ National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, Zhoushan 316022, China

² Marine Science and Technology College, Zhejiang Ocean University, Zhoushan 316022, China

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* gongli1027@163.com

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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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Table 1. List of 22 Cynoglossidae species and two outgroups used in this paper

Name	Abbreviation	AT/%	AT-skew	GC-skew	Length/bp	Accession No.	Reference
Cynoglossus puncticeps	C. pun	62.0	0.012	−0.237	17 158	OP_573760	this study
Paraplagusia bilineata	P. bil	60.2	0.025	−0.225	16 985	NC_023227	unpublished
Cynoglossus monpus	C. mon	61.2	0.007	−0.239	16 425	MT798589	Wang et al., 2020a
Cynoglossus joyneri	C. joy	60.4	0.022	−0.239	16 428	NC_030256	Bo et al., 2017
Cynoglossus melampetalus	C. mel	61.0	0.029	−0.278	16 641	MN082377	Gong et al., 2020
Paraplagusia blochii	P. blo	60.1	0.012	−0.216	16 611	NC_023228	Li et al., 2016
Cynoglossus robustus	C. rob	59.9	0.012	−0.244	16 720	LC482305	Song et al., 2019b
Cynoglossus interruptus	C. int	60.6	0.007	−0.239	17 262	LC482306	Song et al., 2019a
Paraplagusia japonica	P. jap	59.6	0.019	−0.216	16 694	NC_021376	Si et al., 2017
Cynoglossus abbreviates	C. abb	60.4	0.025	−0.259	16 417	JQ349004	Shi et al., 2016a
Cynoglossus roulei	C. rou	60.8	0.028	−0.273	16 598	MN966658	Wang et al., 2020b
Cynoglossus nanhaiensis	C. nan	60.0	0.012	−0.243	17 130	MT117229	Tian et al., 2020
Cynoglossus gracilis	C. gra	61.6	0.019	−0.248	16 565	KT809367	Wei et al., 2016
Cynoglossus semilaevis	C. sem	60.6	0.029	−0.265	16 731	EU366230	Kong et al., 2009
Cynoglossus trigrammus	C. tri	60.6	0.057	−0.304	18 369	KP057581	Mu et al., 2015
Cynoglossus sinicus	C. sin	60.8	0.035	−0.252	16 478	JQ348998	Shi et al., 2015b
Cynoglossus senegalensis	C. sen	59.9	0.044	−0.240	16 519	NC_045034	Gietbong et al., 2018
Cynoglossus bilineatus	C. bil	59.8	0.068	−0.240	16 454	NC_023226	Shi et al., 2016b
Cynoglossus itinus	C. iti	58.8	−0.007	−0.201	16 915	NC_023446	unpublished
Cynoglossus zanzibarensis	C. zan	57.5	−0.003	−0.193	16 569	NC_030364	Shi et al., 2014b
Symphurus orientails	S. ori	58.5	−0.042	−0.177	17 498	KP992899	Shi et al., 2015a
Symphurus plagiusa	S. pla	53.8	0.010	−0.240	17 034	JQ639061	Shi et al., 2015a
Zebrias crossolepis	Z. cro	54.6	0.037	−0.320	16 734	KJ433564	Gong et al., 2016
Zebrias zebrinus	Z. zeb	54.8	0.049	−0.326	16 758	JQ700100	Wang et al., 2013

Table 2. The start codon and stop codon of 13 PCGs in Cynoglossidae mitogenomes

Species	Start codon / Stop codon
Species	ND1	ND2	COⅠ	COⅡ	ATP8	ATP6	COⅢ	ND3	ND4L	ND4	ND5	ND6	Cyt b
Cynoglossus puncticeps	ATG/TAA	ATG/TAA	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TAA
Praplagusia bilineata	ATG/TAA	ATG/T	GTG/TAA	ATG/T	ATG/TAA	ATA/TAA	ATG/TA	ATA/T	ATG/TAA	ATG/TAG	ATG/TAA	ATG/TAA	ATG/TAA
Cynoglossus monopus	ATG/TAA	ATG/TAA	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/TAA	ATG/TAA	ATG/TAG	ATG/TAG
Cynoglossus joyneri	ATG/TAA	ATG/TAA	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/T	ATG/TAA	ATG/TAG	ATG/T
Cynoglossus melampetalus	ATG/TAA	ATG/TAA	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATC/T	ATG/TAA	ATG/T	ATG/TAA	ATG/TAG	ATG/TAA
Praplagusia blochii	ATG/TAA	ATG/T	GTG/TAA	ATG/T	ATG/TAA	ATA/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/T	ATG/TAA	ATG/TAG	ATG/TAA
Cynoglossus robustus	ATG/TAA	ATG/TAG	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TAA
Cynoglossus interruptus	ATG/TAA	ATG/TAG	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TAA
Praplagusia japonica	ATG/TAA	ATG/T	GTG/TAA	ATG/T	ATG/TAA	ATA/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TAA
Cynoglossus abbreviatus	ATG/TAA	ATG/TAA	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/TAG	ATG/TAA	ATG/TAG	ATG/TAG
Cynoglossus roulei	ATG/TAA	ATG/TAA	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/T	ATG/TAA	ATG/TAG	ATG/TAA
Cynoglossus nanhaiensis	ATG/TAA	ATG/TAG	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATT/TAA	ATG/TAA	ATG/TAA	ATG/TAA	ATG/TAA	ATG/TAA
Cynoglossus gracilis	ATG/TAA	ATG/TAA	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/T	ATG/TAA	ATG/TAG	ATG/TAA
Cynoglossus semilaevis	ATG/TAA	ATG/TAA	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATA/T	ATG/TAA	ATG/T	ATG/TAA	ATG/TAG	ATG/TAA
Cynoglossus trigrammus	ATG/TAG	ATG/TAA	GTG/TAA	ATG/T	GTG/TAA	ATG/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/TAA	ATG/TAA	ATG/TAG	ATG/TAA
Cynoglossus sinicus	ATG/TAG	ATG/T	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/T	GTG/TAA	ATG/TAG	ATG/TAA
Cynoglossus senegalensis	ATG/TAA	ATG/T	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/T	GTG/T	ATG/TAG	ATG/TAA
Cynoglossus bilineatus	ATG/TAG	ATG/T	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATA/T	ATG/TAA	ATG/TAG	ATG/TAG	ATG/TAA	ATG/TAA
Cynoglossus itinus	GTG/TAA	ATG/TAG	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATT/T	ATG/TAA	ATG/TAG	ATG/AGA	ATG/TAG	ATG/TAA
Cynoglossus zanzibarensis	ATG/TAG	ATG/TAA	GTG/TAA	ATG/T	ATG/TAA	GTG/TAA	ATG/TA	ATG/T	GTG/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TAA
Symphurus orientails	ATG/TAA	ATG/AGA	ATT/TAA	ATG/T	ATG/TAA	ATG/TAA	ATG/TA	ATG/T	ATG/TAA	ATT/TAG	ATG/TAA	ATG/TAG	ATG/T
Symphurus plagiusa	ATG/TAA	ATG/AGA	GTG/TAA	ATG/AGA	ATG/TAA	ATA/TAA	ATG/TAA	ATG/T	ATG/TAA	ATG/T	ATG/TAA	ATG/TAG	ATG/TAA

Table 3. The genetic distance (bottom left) and sequence similarity (upper right) based on COI gene in 22 Cynoglossidae mitogenomes

	C. abb	C. bil	C. gra	C. int	C. iti	C. joy	C. mel	C. mon	C. nan	C. pun	C. rob	C. rou	C. sem	C. sen	C. sin	C. tri	C. zan	P. bil	P. blo	P. jap	S. ori	S. pla
C. abb		80.20	90.00	83.00	79.40	84.00	82.70	81.40	81.40	81.90	83.10	88.80	88.40	80.90	80.60	80.70	80.30	79.90	80.90	80.60	71.90	73.60
C. bil	0.199		81.30	80.30	81.10	82.10	81.30	80.70	80.40	82.70	80.30	81.50	82.10	84.50	83.00	79.90	82.30	78.70	80.50	80.20	72.80	73.50
C. gra	0.100	0.188		82.90	81.80	83.70	84.10	82.00	82.10	82.80	83.00	89.60	89.10	81.20	80.30	80.20	79.90	79.80	81.60	82.00	71.50	73.90
C. int	0.171	0.198	0.172		81.40	83.40	86.40	82.20	81.50	82.70	99.80	82.00	82.20	80.50	80.10	80.50	81.60	80.70	81.60	82.10	70.80	73.40
C. iti	0.207	0.191	0.183	0.187		83.60	81.10	81.10	84.50	82.00	81.40	80.80	80.40	81.60	80.50	79.70	80.50	79.30	80.50	81.10	71.20	74.30
C. joy	0.161	0.180	0.164	0.167	0.165		85.00	84.30	82.90	85.30	83.50	84.00	83.60	83.20	82.10	82.20	81.70	81.60	82.90	83.00	72.20	75.50
C. mel	0.174	0.188	0.160	0.137	0.191	0.151		82.40	81.70	83.60	86.40	83.60	82.90	81.60	81.30	81.50	80.50	80.70	81.40	81.40	72.20	73.40
C. mon	0.187	0.194	0.182	0.179	0.190	0.158	0.177		80.80	84.80	82.10	82.40	81.80	80.70	81.10	80.50	80.20	81.10	82.20	82.20	71.50	72.80
C. nan	0.187	0.197	0.180	0.186	0.156	0.172	0.184	0.193		81.40	81.50	81.60	81.20	80.50	82.00	81.40	80.90	79.10	82.10	81.90	72.10	74.90
C. pun	0.182	0.174	0.173	0.174	0.182	0.148	0.165	0.153	0.187		82.70	82.20	82.10	80.90	80.20	81.00	80.70	81.40	82.90	82.90	72.40	73.60
C. rob	0.170	0.198	0.171	0.002	0.187	0.166	0.136	0.180	0.186	0.174		81.90	82.10	80.50	80.10	80.30	81.60	80.70	81.70	82.10	70.80	73.40
C. rou	0.110	0.183	0.101	0.178	0.190	0.158	0.162	0.174	0.182	0.176	0.179		96.20	80.90	81.80	80.70	79.60	79.60	80.90	81.80	71.30	73.50
C. sem	0.113	0.177	0.106	0.176	0.194	0.161	0.169	0.180	0.185	0.176	0.176	0.038		80.20	80.90	79.90	80.10	79.30	81.60	82.00	70.90	73.50
C. sen	0.192	0.156	0.189	0.196	0.185	0.169	0.185	0.194	0.196	0.193	0.196	0.190	0.196		85.20	79.20	81.40	77.80	79.10	79.50	72.80	72.60
C. sin	0.195	0.171	0.198	0.200	0.196	0.180	0.188	0.190	0.182	0.200	0.200	0.180	0.189	0.149		79.40	81.80	78.80	80.50	79.00	72.30	72.90
C. tri	0.192	0.200	0.198	0.194	0.202	0.177	0.184	0.194	0.185	0.189	0.196	0.189	0.197	0.207	0.205		79.30	79.00	79.70	79.40	71.70	74.00
C. zan	0.200	0.178	0.202	0.185	0.196	0.184	0.196	0.199	0.192	0.194	0.185	0.202	0.197	0.187	0.183	0.206		79.70	80.70	79.50	71.50	74.10
P. bil	0.202	0.214	0.203	0.194	0.208	0.185	0.194	0.190	0.210	0.187	0.194	0.202	0.206	0.224	0.213	0.209	0.204		85.20	86.30	72.30	73.50
P. blo	0.192	0.196	0.185	0.185	0.196	0.172	0.187	0.179	0.180	0.172	0.184	0.189	0.182	0.211	0.196	0.203	0.194	0.149		87.50	72.40	74.20
P. jap	0.195	0.200	0.181	0.180	0.191	0.171	0.187	0.179	0.182	0.172	0.180	0.180	0.178	0.206	0.211	0.207	0.206	0.138	0.126		72.10	73.60
S. ori	0.727	0.720	0.725	0.720	0.725	0.722	0.715	0.731	0.730	0.727	0.721	0.719	0.718	0.727	0.722	0.719	0.732	0.731	0.721	0.714		76.50
S. pla	0.268	0.266	0.267	0.272	0.260	0.250	0.275	0.280	0.256	0.267	0.272	0.266	0.268	0.276	0.274	0.261	0.262	0.271	0.262	0.268	0.726

Note: Abbreviations of species names are presented as that in Table 1.

Fig. 1. The comparison map of all Cynoglossidae mitogenomes. The species order from the outermost to the innermost ring is presented as that in Table 1, taking Cynoglossus puncticeps mitogenome as the reference. Colors of the block denote the degree of sequence similarity.

Fig. 2. The GC-skew value of 13 PCGs of Cynoglossidae mitogenomes. The species order on the horizontal axis is presented as that in Table 1.

Fig. 3. Structure of control region in 22 Cynoglossidae mitogenomes. The colored ovals indicate the tandem repeats; the remaining regions are shown with green boxes. Tandem repeat with copy number exceeding 5 is displayed in the format of (motif)_n.

Fig. 4. Inferred intermediate steps between the gene order of ancestral teleosts and 22 Cynoglossidae mitogenomes. a. The ancestral gene order of teleosts; b. gene order of Synglossus orientalis (Symphurinae) mitogenome; c. gene order of 17 Cynoglossinae mitogenomes; d. gene order of 3 Cynoglossinae mitogenomes.

Fig. 5. The relationship of Cynoglossidae species and intergenic space between tRNA and QIM. G1, G2 and G3 indicate the intergenic space between Q and I, I and M, M and ND2, respectively.

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