Genome Sequencing of the Japanese Eel (Anguilla japonica) for Comparative Genomic Studies on tbx4 and a tbx4 Gene Cluster in Teleost Fishes

Chen, Weiwei; Bian, Chao; You, Xinxin; Li, Jia; Ye, Lizhen; Wen, Zhengyong; Lv, Yunyun; Zhang, Xinhui; Xu, Junmin; Yang, Shaosen; Gu, Ruobo; Lin, Xin; Shi, Qiong

doi:10.3390/md17070426

Cited by 11 publications

(8 citation statements)

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“…Tbx4 stimulates the formation of appendage buds and induces the formation of leg-like structures, while Tbx5 promotes the formation of wing-like appendages, indicating that Tbx4 / 5 might play key roles in limb induction ( Naiche & Papaioannou, 2003 ; Takeuchi et al, 2003 ; Naiche & Papaioannou, 2007 ). Similar mechanisms have been reported in other species, including Notophthalmus viridescens and Anguilla japonica , in which Tbx4 and Tbx5 were reported to be involved in the formation of hind limbs and forelimbs, respectively ( Simon et al, 1997 ; Khan, Linkhart & Simon, 2002 ; Chen et al, 2019 ). Silver pomfret ( Pampus argenteus ) is an economically important fish species, and its nutritive value and medicinal applications are widely known ( Xu et al, 2012 ; Zhang et al, 2014 ).…”

Section: Introductionsupporting

confidence: 83%

Screening and identification of miRNAs regulating Tbx4/5 genes of Pampus argenteus

Zhang

Liu

et al. 2022

PeerJ

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Background Silver pomfret (Pampus argenteus) is one of the most widely distributed and economically important pelagic fish species. However, an unique morphological feature of P. argenteus is the loss of pelvic fins, which can increase the energy requirement during food capture to some extent and is therefore not conducive to artificial culture. Tbx4/5 genes are highly conserved regulatory factors that regulate limb development in vertebrates and are in turn regulated by microRNAs (miRNAs). However, the miRNAs that directly regulate the Tbx4/5 genes in P. argenteus remain to be elucidated. Methods The Tbx4/5 genes of P. argenteus were first cloned, and the small RNA transcriptomes were sequenced by high-throughput sequencing during the critical period of the fin development at days 1, 7, and 13 of hatching. The miRNAs regulating the Tbx4/5 genes of P. argenteus were subsequently predicted by bioinformatics analysis, and the related miRNAs were verified in vitro using a dual fluorescence reporter system. Results A total of 662 miRNAs were identified, of which 257 were known miRNAs and 405 were novel miRNAs were identified. Compared to day 1, 182 miRNAs were differentially expressed (DE) on day 7, of which 77 and 105 miRNAs were downregulated and upregulated, respectively, while 278 miRNAs were DE on day 13, of which 136 and 142 miRNAs were downregulated and upregulated, respectively. Compared to day 13, four miRNAs were DE on day 7, of which three miRNAs were downregulated and one miRNA was upregulated. The results of hierarchical clustering of the miRNAs revealed that the DE genes were inversely expressed between days 1 and 7, and between days 1 and 13 of larval development, indicating that the larvae were in the peak stage of differentiation. However, the number of DE genes between days 7 and 13 of larval development was relatively small, suggesting the initiation of development. The potential target genes of the DE miRNAs were subsequently predicted, and Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses of target genes were performed. The results suggested that the DE miRNAs were involved in growth, development, and signal transduction pathways, of which the Wnt and Fgfs signaling pathways are known to play important roles in the growth and development of fins. The results of dual fluorescence reporter assays demonstrated that miR-102, miR-301c, and miR-589 had a significant negative regulatory effect on the 3′-UTR of the Tbx4 gene, while miR-187, miR-201, miR-219, and miR-460 had a significant negative regulatory effect on the 3′-UTR of the Tbx5 gene. Altogether, the findings indicated that miRNAs play an important role in regulating the growth and development of pelvic fins in P. argenteus. This study provides a reference for elucidating the interactions between the miRNAs and target genes of P. argenteus in future studies.

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Section: Introductionsupporting

confidence: 83%

Screening and identification of miRNAs regulating Tbx4/5 genes of Pampus argenteus

Zhang

Liu

et al. 2022

PeerJ

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“…It can be speculated that Tbx4 is different in different species as certain genes are known to have changed, leading to their evolution and loss of certain functions; However, Tbx4-speci c DNAbinding sites and structures are highly homologous across species, suggesting the importance of Tbx4 function. Interestingly, the complete exon structure of Tbx4 was also found in in several pelvic-n-loss species such as Mola mola and Monopterus albus [32].…”

Section: Discussionmentioning

confidence: 79%

Tbx4 and Tbx5 gene expression associated with appendage development and its relationship with the absence of a ventral fin in Pampus argenteus

Zhang

Zhu

et al. 2022

Preprint

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Background The Tbx family was first known through the study of their functions in the body and limbs, and its members Tbx4 and Tbx5 genes are important factors in determining the characteristics of the appendages. Pampus argenteus is an important fishery resource and an emerging target of aquaculture. It has a bizarre morphology, the lack of ventral fin. So, it is necessary to study the role of Tbx family genes in the deletion of pelvic fin in P. argenteus. Results Cloning Tbx4 and Tbx5 cDNA sequence of P. argenteus for the first time (GenBank: MH709128 and MH712458), which both contain highly conserved T-box region (DNA binding domain). In different developmental stages of P. argenteus, the expression of Tbx4 mRNA showed an overall "M" trend of increasing, then decreasing and then increasing again, with the highest peak at the age of 13 days old larvae; and a positive RNA hybridization signal was detected in the abdominal epithelium, while its protein expression was significantly inhibited. TBX4 protein expression was lowest in the abdominal epithelium and even inferior to its expression in the pectoral fin. At different developmental stages of P. argenteus, the expression of Tbx5 mRNA showed an overall trend of first increase and then decrease, and reached the highest at larvae 1 day (the appearance of pectoral fin primordium). Consistent with in situ hybridization, positive signals were concentrated in the heart and pectoral fins. The expression of TBX5 protein is basically consistent with the expression of mRNA, that is, when the expression of Tbx5 mRNA increases, its protein content also increases relatively, and after accumulation to a certain extent, the accumulation of pectoral fin cells begins to appear. Conclusions The translation of Tbx4 mRNA may be inhibited during the critical period of ventral fin development. Among different tissues, TBX4 protein levels were the lowest in the abdominal epithelium, and even lower than that in the pectoral fin, suggesting that the protein expression may be also inhibited in the abdominal epithelium of adult P. argenteus.

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“…This chromosome rearrangement resulted in the same haploid chromosome number (n = 25) in tarpons. Comparatively, the 19 AETK's chromosomes (Chr1, 2, 4, 7, 9-14, 16-21, 23-25) underwent 24-fusion and 18-fission to form the 13 chromosomes (Chr1- 8,11,13,[15][16][17] in Japanese eels (Supplementary Table 14). The…”

Section: Supplementary Tables 4)mentioning

confidence: 99%

“…A draft genome of the American eel (with a total size of 1.41 GB) was published in 2017, and 26,564 genes were annotated 73 . In 2019, the assembly of a Japanese genome of 1.13 Gb 17 was improved with 256,649 contigs, 41,687 scaffolds, and a scaffold N50 of 1.03M. Currently, only the draft genome is available for Japanese eels.…”

Section: Introductionmentioning

confidence: 99%

A Chromosome-level Assembly of the Japanese Eel Genome, Insights into Gene Duplication and Chromosomal Reorganization

WANG

Wan

et al. 2022

Preprint

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Japanese eels (Anguilla japonica) are commercially important species that have been harvested extensively for foods. Currently, this and related species (American and European eels) are difficult to breed on a commercial basis. Wild stock is used for aquaculture. Due to pollution, overfishing, and international trafficking, eel populations are declining. The International Union for Conservation of Nature lists Japanese eels as critically endangered and on its red list. Here we presented a high-quality genome assembly for Japanese eels and demonstrated that large chromosome reorganizations occurred in the events of third-round whole-genome duplications (3R-WRD). Following multiple chromosomal fusion and fission rearrangement, the Anguilla lineage has reduced the haploid chromosomal number of 19 from the ancestral proto-chromosomal number of 25. Phylogenetic analysis of expanded gene families showed the gene families of olfactory receptors and voltage-gated Ca2+-channel expanded significantly. The expansion of olfactory receptors (group delta and zeta genes) and voltage-gated Ca2+-channel gene families are important for olfaction and neurophysiological functions. Following 3R-WGD, additional tandem (TD) and proximal (PD) duplications occurred to acquire immune-related genes for adaptation. The Japanese eel assembly presented here can be used to study other Anguilla species that are related to evolution and conservation.

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Genome Sequencing of the Japanese Eel (Anguilla japonica) for Comparative Genomic Studies on tbx4 and a tbx4 Gene Cluster in Teleost Fishes

Cited by 11 publications

References 84 publications

Screening and identification of miRNAs regulating Tbx4/5 genes of Pampus argenteus

Screening and identification of miRNAs regulating Tbx4/5 genes of Pampus argenteus

Tbx4 and Tbx5 gene expression associated with appendage development and its relationship with the absence of a ventral fin in Pampus argenteus

A Chromosome-level Assembly of the Japanese Eel Genome, Insights into Gene Duplication and Chromosomal Reorganization

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