apostichopus japonicus

Res. Angerer, L. M. et al. 14, 375388 (2000). Limnol. & Smyth, G. K. edgeR: A bioconductor package for differential expression analysis of digital gene expression data. While circadian regulation has been extensively studied in many organisms, the exact ways of how these key regulators exert their effects in sea cucumbers aestivation and whether in the same way as in circadian regulation remain to be thoroughly explored. [3] The red morphs are found on gravel beds offshore at depths of 40 metres (130ft) or deeper while the other two colours are found intermingled on muddy and sandy bottoms at shallower depths. 2b), and they are also the only two genes significantly expressed in sea urchin embryos44. Defensive mechanisms and ecology of some tropical holothurians. Compared to the inferred ancestral bilaterian LAS sequence (see Methods for details), LAS1 and LAS2 in sea cucumber show the highest sequence divergence and possess more putative plant sites than most other animals. J. The sea cucumber Apostichopus japonicus is a foodstuff with very high economic value in China, Japan and other countries in south-east Asia. Understanding mechanism of sea cucumber Apostichopus japonicus aestivation: Insights from tmt-based proteomic study. Jin.W. Illumina mate-paired DNA sequencing-library preparation using cre-lox recombination. 6, 893904 (2005). Raw reads were first preprocessed to remove any sequences with ambiguous basecalls (N), long homopolymer regions (>10bp) and excessive low-quality positions (>20% positions with quality score<10). Commun. As both sterols and triterpenes are synthesized via the mevalonate (MVA) pathway49, we first investigated the integrity of the MVA pathway in sea cucumber for the route of cholesterol synthesis in animals, and we found that the two genes Cyp51 and Dhcr7 were absent in the sea cucumber genome (Fig. The Japanese sea cucumber Apostichopus japonicus plays important ecological and economic roles in the coastal areas of Japan. The immune gene repertoire encoded in the purple sea urchin genome. We thus suggest aqua-farmers carry out seeding at night in stock enhancement. Zhang, Q. 39, 139165 (2005). 4c; Supplementary FigureS16), and is re-activated with emerging arousal from aestivation (corresponding to the decreasing effect of Cry1; Fig. Sea cucumber genome provides insights into saponin - PubMed Klf2 and Egr1 are recognized as hub transcription factors in the network. volume4, Articlenumber:29 (2018) Biol. Sequencing reads were aligned to the A. japonicus genome using STAR aligner92 with its default parameters. Chen, M. et al. PLoS Genet. The circle size and filled portion represent the gene numbers (from the AM7 module) and percentage of differentially expressed genes (DGEs) in a given pathway, respectively. Gene-specific primers were designed using Primer Premier 5.0, and the primer sequences are listed in Supplementary TableS26. b Expression profiles of nine TFs showing differential expression during aestivation in all four organs. Known genes participating in the human MVA pathway were downloaded from NCBI protein database and aligned to the full gene sets of three echinoderms (A. japonicus, S. purpuratus and A. planci) by BLASTP with 1e-5. and JavaScript. USA 95, 1306213067 (1998). Genes Dev. Dev. Chappell, J. PubMed Seasonal variations of food sources in Apostichopus japonicus indicated by fatty acid biomarkers analysis. Mito, T. & Endo, K. PCR survey of Hox genes in the crinoid and ophiuroid: Evidence for anterior conservation and posterior expansion in the echinoderm Hox gene cluster. Meng, Q. et al. Kato and Hirata (1989) outlined two types of circadian rhythms in Apostichopus (as Stichopus) japonicus from laboratory work in Japan. Nat. Dev. Adult sea cucumbers (70100g) were collected from the coast of Liaoning, China (1213347E, 385155N) and acclimated in seawater aquaria (~500l) at 15C for 2 weeks prior to treatment, while being fed mixed feed once a day. Evolutionary distances were computed using the p-distance method100. Stat. [as Stichopus japonicus p . Aestivation states: non-aestivation (Non_aes); early aestivation (Early_aes); deep aestivation (aes); and arousal from aestivation (Aro). Due to the unsatisfactory scaffolding efficiency of PacBio long reads for the sea cucumber genome8, we also adopted a classic strategy using traditional mate pair sequencing in the scaffolding step. Fish. The extract was then dried down and the residue was dissolved in 500l of hexane. [8] This sea cucumber has been known to continue in aestivation in some areas of China for four years. Food Sci. [3] Rocks and tiles are placed on the bottom to provide settlement for larvae and protection from predators. Statistical analyses of the data were performed with the SPSS (version 16.0) statistical software package using independent t-tests. Toralgranda, V., Lovatelli, A. Fold-change (regeneration stages vs. the control stage) is color-coded. 9, a022137 (2017). HMGs are involved in numerous metabolic pathways, suggesting that intestine hypometabolism is caused by transcriptional suppression of metabolic pathways mediated through DNA hypermethylation. . [3], The sexes are separate in the Japanese sea cucumber. Consortium, S. U. G. S. et al. Apostictopterus fuliginosus. Nei, M. & Kumar, S. Molecular evolution and phylogenetics. Mar. Embryos (zygote, blastulae and gastrulae), larvae (auricularia, doliolaria, and pentactula) and juveniles of A. japonicus were collected based on artificial fertilization of sex-matured adults and larval cultivation according to Zhang et al.91. Bioinformatics 29, (1521 (2013). Mitsukuri, K. 1912. A Novel Full-Length Transcriptome Resource for Sea Cucumber Article Yuq.L. The remaining animals were subjected to a decrease in water temperature back to 18C (at a rate of 0.5C per day), held at 18C for 2 days and then sampled as the arousal-from-aestivation group105. The sea cucumber genome, together with extensive transcriptomes, represents an invaluable resource and provides a new avenue for understanding the evolutionary appearance and molecular regulation of these extraordinary biological features in sea cucumbers and other echinoderms. Part. The supplements included the following: ergosterol (Fluka), 20g/ml; hemin (Sigma-Aldrich), 13g/ml; and Tween- 80 (Sigma-Aldrich), 5mg/ml. The largest fishery is in Japan where between 2000 and 2005, an average of 8,101 tonnes of this species were harvested annually. For each state, transcriptome sequencing was independently conducted for two to three individuals (i.e., biological replicates) to ensure reliable quantification of gene expression. 8, 1721 (2017). They were then pelleted and washed once with ddH2O before triterpene extraction. Directed acycline graphs (DAG) of GO terms corresponding to biological process were generated using OmicShare tools (www.omicshare.com/tools). Echinoderms, albeit evolving from the same bilaterian ancestor that gave rise to chordates, display a variety of highly derived, Cambrian-derived body architectures36 for which the molecular driving force(s) remain poorly understood37. 207, 450460 (1996). Cytom. The Fgfr gene family shows significant expansion in the sea cucumber genome (38 in contrast to 413 in other echinoderms or chordates). A. japonicus is dioecious, and no phenotypic differences between males and females can be detected before sexual maturation. Yul.L., Jin.W., S.W. https://doi.org/10.1038/s41421-018-0030-5, DOI: https://doi.org/10.1038/s41421-018-0030-5. BMC Bioinforma. Nat. G protein-coupled receptor (GPCR)-mediated signaling systems might play critical roles in the reproductive control of A. japonicus. Given the importance of this species in aquaculture, accurate determination of its natural diet and feeding strategy will facilitate development of artificial diets for it. 11 (Academic Press, United States, 2015). Apostichopus japonicus - an overview | ScienceDirect Topics The intestine regeneration involves diverse signaling pathways including Wnt, Hippo and FGF. Liu, Y. T., Hu, T. C., Chang, C. H., Shie, W. S. & Wu, T. K. Protein engineering of Saccharomyces cerevisiae oxidosqualene-lanosterol cyclase into parkeol synthase. Kume, K. et al. The sites detected in at least one group of three samples with coverage>2 were used for differential DNA methylation analysis. In addition, the absence of Cyp51 (i.e., C-14 sterol demethylase) in the sea cucumber genome also supports the previous speculation that the blockage of C-14 demethylation leads to the accumulation of 14-methylated 9(11)-sterols in cell membranes of sea cucumber, contributing to resistance to their own toxins15. The sea cucumber genome contains 254Mb of repetitive sequences accounting for 26% of the genome. A.O. We identified 6,511 DGEs (Supplementary TablesS32, S33; Supplementary FigureS19), and co-expression network analysis identified two regeneration-related modules that involved diverse signaling pathways, including Wnt and Hippo, which are well-known for participating in intestine regeneration in sea cucumber and other animals69,70 (Supplementary Figures S20-S24; Supplementary TablesS34-S36). Adv. Z.B., S.W., Y.C. The Journal of the College of Science, Imperial University of Tokyo.39: 1-284. These unclassified elements were further classified using the following strategy: (a) Unknown repeat sequences were aligned to Repbase using blastn; (b) Remaining unknown repeats were aligned to RepBase using tblastx; (c) Remaining unknown repeats were aligned to Uniprot database; and (d) Remaining repeats were classified by TE-class using multiple classification methods. 27, 168173 (2001). Inhibition of erg11 might lead to an accumulation of LAS1 products without further modifications. Anders, S., Pyl, P. T. & Huber, W. Htseq--a python framework to work with high-throughput sequencing data. & Cameron, R. A. Paleogenomics of echinoderms. & Dolmatov, I. Y. Regeneration of the digestive tube in the holothurian Apostichopus japonicusafter evisceration. Dynam. BLAST hits in every echinoderm species were further checked by domain searching to ensure the presence of expected protein domains. Ecol. Y.W. Their superb adaptation attributes include several fascinating evolutionary innovations that are rarely seen in the animal kingdom such as a pentaradial body plan with rigid calcitic skeletons4, biosynthesis of saponins5, and extraordinary potential for regeneration6. Commun. Frontiers | Effects of sea urchin feces on behaviors, digestion ability AjTGF alleviates V. splendidus-induced inflammation through SMADs The hubness of a gene in the aestivation-related module (AM7) was measured by its connection strength with other genes in the module and was determined by intra-modular connectivity (Kwithin)109. It is ubiquitously detectable in oceans and affects a variety of marine animals. All positions containing gaps and missing data were eliminated and the robustness of the resulting phylogenies was tested by a reanalysis of 1,000 bootstrap replicates101. To understand the phylogeny of Fgfr genes of A. japonicus, the homologs from several selected animals including sea urchin (S. purpuratus), scallop (C. farreri), human (H. sapiens), mouse (M. musculus), chicken (G. gallus) and zebrafish (D. rerio), were retrieved from NCBI (http://www.ncbi.nlm.nih.gov) and Ensembl (http://useast.ensembl.org). Hibino, T. et al. Toxins. By taking advantage of both Illumina short-read and PacBio long-read sequencing technologies, we performed whole-genome shotgun sequencing of a wild individual of A. japonicus, which produced 352Gb of clean data, corresponding to an average genome coverage of 370 (Supplementary TableS1). and W.L. Biotechnol. the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Thank you for visiting nature.com. Nature 544, 231234 (2017). Apostichopus japonicus is a species of sea cucumber in the family Stichopodidae. We found that intestine hypometabolism during aestivation is driven by the DNA hypermethylation-mediated expression suppression of various metabolic gene pathways, providing direct evidence linking DNA methylation with hypometabolism. The extraordinary ability of saponin synthesis in sea cucumber is enabled by its modification of lanosterol synthase, which possibly occurred through convergent evolution. D 22, 3238 (2017). Star: Ultrafast universal rna-seq aligner. The AM7 module governs diverse gene pathways, including those participating in cell proliferation and differentiation, seasonal rhythmicity and immune responses, suggesting the complex mechanism of molecular regulation during sea cucumber aestivation. Zimin, A. V. et al. Google Scholar. For each state, total mRNA was extracted from body wall using an RNeasy Lipid Tissue Mini Kit (QIAGEN). We also revealed that the spatial expression patterns of Hox7 and Hox11/13b were potentially responsible for embryo-to-larva axial transformation in echinoderms. f Expression of the FGF signaling pathway72 during intestine regeneration in sea cucumber. 225, 275286 (2015). The genome size was estimated using the following formula:77 genome size=(total number of 19-mers)/(position of peak length). The potential roles of the FGF signaling pathway in intestine regeneration are supported by observation of the activation of various downstream cascades during the intestine regeneration process in sea cucumber. The amino acid percentage in every remaining position was calculated for plant BAS genes, plant CAS genes and animal LAS genes. Abstract. PubMed Central Evol. It contains only one species, Apostictopterus fuliginosus, which is found in India ( Assam) and West China. The intestine of sea cucumber shows prominent hypermethylation during aestivation. PubMed Sci. Google Scholar. The feed ingredients included fresh sea mud (40%), Sargassum thunbergii (30%), and sea cucumber compound feed (30%, An-yuan company, China). Biol. CAS Evol. Wang, S. et al. Fish. Background Apostichopus japonicus is an economically important species in the global aquaculture industry. Nine TFs showed differential expression during aestivation in all four organs, of which Klf2 and Egr1 were the most significant TFs especially in body wall (Fig. Dardente, H., Hazlerigg, D. G. & Ebling, F. J. P. Thyroid hormone and seasonal rhythmicity. participated in initial genome analysis. The ancestral animal sequence of the LAS gene was deduced based on the following criterion: the amino acid was the predominant type in at least two of three animal groups (non-bilaterian, protostomia and deuterostomia). C.M. Apostichopus japonicus is a common temperate species of sea cucumber found in the northwest Pacific ( Liao, 1980; Sloan, 1984) (see Chapter 3 for details on its geographic distribution). The distribution of 19-mers was calculated based on paired-end reads derived from the DNA libraries with insert sizes of 180bp, 350bp and 500bp. Saponins are widespread in plants but are rarely found in the animal kingdom19,20, and how sea cucumbers gained the ability to synthesize saponins remains enigmatic. Aestivation states are the same as depicted in (b) except Pre_aro representing initial arousal from aestivation. Cell. 9, R7 (2008). Ch. Bottjer, D. J., Davidson, E. H., Peterson, K. J. This hypothesis was, however, recently challenged by the finding of an intact Hox cluster in the sea star Acanthaster planci37,41. Biochem. 74.S1). These animals can be spawned from July . To understand the gene regulatory network of aestivation, we constructed a gene co-expression network using the 39 transcriptome data sets, and identified 6 aestivation-related modules, with AM7 as the most significant module across three organs (body wall, muscle and respiratory tree; Supplementary FigureS17; Supplementary TableS27). It summarizes the historical and most recent developments in the trade and aquaculture of . Biol. The protein sequences of the selected species were aligned to the repeat-masked sea cucumber genome using the Exonerate89 tool with parameters of --model protein2genome --refineboundary 1000 --showvulgar no --showalignment no --showquerygff no --showtargetgff yes. Fao Fish. Dev. Intestinal hypometabolism during aestivation is driven by the DNA hypermethylation of various metabolic gene pathways, whereas the transcriptional network of intestine regeneration involves diverse signaling pathways, including Wnt, Hippo and FGF. The open reading frames (ORFs) of OSCs were amplified from gblocks using the oligonucleotides listed in Supplementary TableS19. 10.2305/IUCN.UK.2013-1.RLTS.T180424A1629389.en, "Population status, fisheries and trade of sea cucumbers in Asia". The sea cucumber lacks two genes, Cyp51 and Dhcr7, suggesting that it might have lost its de novo cholesterol synthesis ability, consistent with the previous observation of extremely low cholesterol content in sea cucumber50. Transcriptomic and Metabolomic Analyses Provide Insights into the Real-time PCR was conducted using the SYBR Premix Ex Taq II (Tli RNaseH Plus) on an ABI7500 real-time PCR System. CAS Gene expression levels in terms of RPKM were estimated by HTseq93 and custom Perl scripts. Progressively restricted expression of a homeo box gene within the aboral ectoderm of developing sea urchin embryos. Construction of a high-density genetic map and quantitative trait locus mapping in the sea cucumber Apostichopus japonicus. Tao, W. et al. AjSMAD 2/3 silencing alleviated rAjTGF--induced damage recovery. Ornitz, D. M. & Itoh, N. The fibroblast growth factor signaling pathway. To define the effect of the sea cucumber intestine extracts on the body wall, the intestinal extracts and crude collagen fibers (CCF) of sea cucumber A. japonicus were prepared. provided computational services and technical support. Journal of Ocean University of China, 13(2): 303-310. After acclimation, the regeneration group (30 sea cucumbers) was treated to induce evisceration by intra-coelomic injection of 0.35M KCl. Apostictopterus - Wikipedia DNA transposons represent the most abundant repeat type (3.5%), followed by long interspersed elements (2.1%) and tandem repeats (2.0%) (Supplementary TableS9; Supplementary FigureS5). Extreme genomic variation in a natural population. Polymorphism analysis identified 2.43 million single-nucleotide polymorphisms (SNPs) in the assembled individual. Dev. Krzywinski, M. et al. B. In Russia and North Korea, overfishing has reduced populations considerably. Nucleic Acids Res. Bull. [4] In lagoons in southern Sakhalin, Russia, Japanese spiky sea cucumber are found on solid substrates among growth of the red alga Ahnfeltia tobuchiensis and in oyster beds (Crassostrea gigas). [8] Hatchery techniques are being developed in Japan and China as are the preparation of suitable culture feeds and the investigation of the best methods of ranching. Bootstrapping with 1000 replications was conducted to evaluate the robustness of the phylogenetic tree. (2015) and Liu, Sun, Ru, Hamel, and Mercier (2015). Bakus, G. J. Biol. Gene expression levels in terms of RPKM were estimated by HTseq93 and custom Perl scripts. SNP density in coding sequences (CDSs) varies dramatically among genes, ranging from 0 to 222 SNPs per kb (Fig. RepeatMasker was used for homology-based transposable element (TE) prediction: we ran searches against RepBase sequences with default parameters83. The Japanese sea cucumber has a cylindrical leathery body with blunt, thorny protuberances. Nat. Gene expression levels in terms of RPKM were estimated by HTseq93 and custom Perl scripts. Body wall showed the most differential expressed genes (DEGs) and differentially expressed transcriptional factors (DE-TFs), followed by muscle, respiratory tree and intestine (Fig. Consequently, we constructed short-insert paired-end libraries (180bp, 350bp, 450bp, 500bp and 550bp) using the Illumina standard protocol (San Diego, USA) and long-insert mate-pair libraries (5Kb, 10Kb, 15Kb and 20Kb) following the Cre-lox recombination-based protocol74. Total mRNA was extracted following the protocol described by Du et al27. Comp. Evol. These HPGs may contribute to the sea cucumbers superb adaptation by enhancing the plasticity of its coding repertoire. Genome Res. The authors declare that they have no conflict of interest. USA 109, 1090310908 (2012). Z.B., S.W., Y.C., Zu.Z., R.W., Yul.L. Sequencing reads were aligned to the A. japonicus genome using STAR aligner92 with its default parameters. All RNA-seq libraries were constructed using the NEB Next mRNA Library Prep Kit by following the manufacturers instructions and then were subjected to paired-end 100-bp (PE100) sequencing on the Illumina HiSeq 2000 platform. Study on aestivating habit of sea cucumber Apostichopus japonicus selenka: the factors relating to aestivating. All experiments were repeated to confirm the reproducibility of triterpene profiles. 12, e1006433 (2016). Sea cucumber LAS1 produces parkeol (previously identified as the triterpene precursor of sea cucumber saponins;51), whereas LAS2 produces 9-lanosta-7, 24 dienol. Annu. participated in genome sequencing, assembly and annotation. Genet. & Franco, C. M. Acetylated triterpene glycosides and their biological activity from holothuroidea reported in the past six decades. At the anterior or front end there is a mouth surrounded by a ring of short feeding tentacles and at the posterior end is the anus. AjTGF- mRNA levels displayed higher abundance in body wall. In total, 29,451 protein-coding genes were retained, constituting the final gene set of A. japonicus. & Chen, M. Differential gene expression in the respiratory tree of the sea cucumber Apostichopus japonicus during aestivation. [3], The Japanese sea cucumber is found along the coast of Russia, China, Japan and Korea. Our analysis revealed novel genomic features and molecular changes that may contribute to the evolutionary innovations of sea cucumber or echinoderm-characteristic adaptive traits, providing insights into saponin synthesis and aestivation regulation. Japanese Spiky Sea Cucumber articles - Encyclopedia of Life Here, we report sequencing of the genome and extensive transcriptomes of A. japonicus. The genome of the sea urchin Strongylocentrotus purpuratus. Kelly, M. S. Echinoderms: Their culture and bioactive compounds. Shannon, P. et al. Wires Dev. The sea cucumber Apostichopus japonicus is one of the primarily commercialized marine species with high output value and profit in China ( Hair et al., 2012; Han et al., 2016 ). Baughman, K. W. et al. Automated eukaryotic gene structure annotation using evidencemodeler and the program to assemble spliced alignments. Several individuals were maintained as the non-aestivation control group, and the other were slowly induced into aestivation by increasing the water temperature from 15C to 25C at a rate of 0.5C per day. Phylogenetic trees were constructed using MEGA7 with the Neighbor-Joining method98,99. The threshold temperature is about 25C (77F), higher for smaller individuals and for those from the southern part of the range where the ambient water temperature is higher. a global review of fisheries and trade. & Vasconcellos, M. Sea cucumbers. participated in gene network analysis. d The phylogeny of the Fgfr gene family in sea cucumber and other animals. (Cold Spring Harbor Lab. The injector port, source and transfer line temperatures were set at 250C and an oven temperature program from 80C (2min) to 290C (30min) at 20C/min was used. PubMed Zhang, L. et al. Lih.Z., H.L. 4, 1385 (2013). The TFs showing differential expression in all organs are labeled in red, whereas for the remaining DE-TFs showing differential expression in at least one organ are labeled in yellow. 10, 516518 (2008). Bioinformatics 29, 26692677 (2013). Nuclear DNA content and genome size of trout and human. The total assembly length was close to the estimates from k-mer analysis (~1.0Gb; Supplementary FigureS2) and flow cytometry analysis35 (~0.9Gb; Supplementary FigureS3). Hao Song, in Developments in Aquaculture and Fisheries Science, 2015. Sea cucumber genome provides insights into saponin - Nature Scallop genome provides insights into evolution of bilaterian karyotype and development. Radical alterations in the roles of homeobox genes during echinoderm evolution. Liu, J. et al. Cameron, R. A., Kudtarkar, P., Gordon, S. M., Worley, K. C. & Gibbs, R. A. a Identification of differentially methylated sites during different aestivation states. Sterols and triterpenes share the common biosynthetic precursor 2,3-oxidosqualene, which can be cyclized by different oxidosqualene cyclases (OSCs) to produce sterols [lanosterol synthase (LAS) in fungi and animals and cycloartenol synthase (CAS)/cucurbitadienol synthase (CPQ) in plants] or triterpenes [e.g., -amyrin synthase (BAS) in plants]20 (Fig. Cytoscape108 was employed for visualization of the co-expression networks. After quality filtering, 352.38Gb of high-quality data were used for genome assembly. The non-redundant consensus set of gene structures was integrated in EVidenceModeler (EVM)90 using all the gene evidence predicted above with parameters of --segmentSize 100000 --overlapSize 10000. R.W., T.L., H.S. We have previously grown Apostichopus japonicus triploids with a growth advantage. Guillaumond, F. et al. Internet Explorer). 18, 164179 (2017). PLoS ONE 5, e15633 (2010). To identify the Hox and ParaHox genes, homeodomains were searched in the A. japonicus genome using BLAST with an E value threshold of 1e5 against all homeodomain sequences retrieved from the HomeoDB database (http://homeodb.zoo.ox.ac.uk/)97 and were further confirmed by comparing the results to the Conserved Domains Database (http://www.ncbi.nlm.nih.gov/cdd). Differentially expressed genes (DEGs) and differentially expressed TFs (DE-TFs) were detected using the edgeR package (p<0.05)106. Russian A. japonicus , mainly harvested in the Vladivostok region, exhibits significant . Lanosterol (Cat# L5768) was purchased from Sigma-Aldrich, whereas parkeol and lanostadienol were purified and characterized according to published literatures103,104. MOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao, 266003, China, Yuli Li,Ruijia Wang,Xiaogang Xun,Jing Wang,Tianqi Li,Jia Lv,Chuang Mu,Xiaoli Hu,Lingling Zhang,Jing Liu,Yuqiang Li,Lijie Yao,Wenqian Jiao,Yangfan Wang,Shanshan Lian,Xiaoting Huang,Huan Liao,Jia Wang,Hongzhen Sun,Xue Mi,Yu Xia,Qiang Xing,Wei Lu,Zhenmin Bao&Shi Wang, Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China, The Ben May Department for Cancer Research, The University of Chicago, Chicago, IL, 60637, USA, Department of Metabolic Biology, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom, College of Fisheries and Life Science, Dalian Ocean University, Dalian, 116023, China, Jun Ding,Liheng Zhang,Yaoyao Zhan&Yaqing Chang, Liaoning Key Lab of Marine Fishery Molecular Biology, Liaoning Ocean and Fisheries Science Research Institute, Dalian, 116023, China, Jingwei Jiang,Zelong Zhao&Zunchun Zhou, Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China, You can also search for this author in
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