In this cluster, the genes were arranged with 11 tandem duplications that had no homologs in other species and contained highly conserved cysteine residues, which suggested that they may belong to a gene family specific to A. japonicus. Evisceration was induced by injecting about 2 mL 0.35 molL-1 KCl into the coelom. Raw sequencing data of transcriptomes have been deposited in NCBI under the accession number SRR5083072-SRR5083088. Methods and Resources report novel methods, substantial improvements to current methodologies, or informational datasets. However, the number of downstream biomineralization genes is significantly different between the sea urchin and the sea cucumber. The stomochord was considered as the supporting organ of hemichordates, even though no molecular evidence of homology has been detected between stomochord and notochord [28,29]. Department of Biology, Carleton University, Ottawa, Ontario, Canada, Roles Compared with sea urchin, there is a significant gene loss in the A. japonicus genome, and the expression levels for those genes at different development stages are relatively low. There are 763 gene families shared by 3 echinoderms. The information provided in the figure for each category is the expression profile in each regeneration stage. Yes An exact heterozygous rate of 1.59% was estimated, which was close to the evaluation by simulated k-mer distribution. cytochrome P450 family 2; DBG2OLC, $88.00. sea translation in English-Northern Sami dictionary. Long bars represent scaffolds with a length > 500 Kb; short bars represent scaffolds with a length ≤ 500 Kb. A total of 30,350 protein-coding gene models were constructed, and among them, 28,144 (92.73%) were supported by the transcriptome data. A local repeat library of 1,507 sequences was produced by RepeatModeler and was used for the following prediction [76]: All major classes of TEs were summarized and compared with S. purpuratus (S7 Table). Another cluster with 21 tandem-duplicated FREP genes was located on Scaffold75. Sea cucumber is rich in chondroitin sulfate, which is well-known for … The genes connected on a line indicate that they are clustered in order in the genome. An integrated multiomics approach offered insight into the genome architecture of sea cucumbers and the genetic underpinnings of their unique biological traits. https://doi.org/10.1371/journal.pbio.2003790.s042, https://doi.org/10.1371/journal.pbio.2003790.s043, https://doi.org/10.1371/journal.pbio.2003790.s044, https://doi.org/10.1371/journal.pbio.2003790.s045. In the A. japonicus genome, we found a single, substantially intact, and well-ordered Hox gene cluster containing 10 Hox genes, as well as a conserved ParaHox gene cluster (Fig 4) and large numbers of other homeobox genes (S17 Table). Corresponding proteomic studies confirmed that these factors may play important roles in this process (S22–S24 Tables). Echinoderms may also reproduce asexually, as well as regenerate body parts lost in trauma. Total RNA was extracted using the TRIzol extraction method (Thermo Fischer Scientific, Germany) according to the manufacturer’s protocol. Received by HY and SJ. https://doi.org/10.1371/journal.pbio.2003790.s015. (A) Plot of the second important axis (Axis2) after correspondence analysis against the codon adaptive index (CAI). The Scaffold889 with 11 tandem-duplicated genes (blue asterisk) shows significant up-regulation post evisceration. For more information about PLOS Subject Areas, click Track 4: distributions of 5 significantly expanded gene families in the genome. Objective: The identification of the active phenolic compounds in the mixed extract of sea cucumber (Holothuria atra) body wall by high-performance liquid chromatography and an assessment of its hepatoprotective activity against thioacetamide-induced liver fibrosis in rats. Received by LZ, CLin, and HY. PLOS Biology provides an Open Access platform to showcase your best research and commentary across all areas of biological science. A total of 452 gene families were shared by A. japonicus and S. purpuratus (Fig 2B), many of them enriched in metabolism pathways of glycerophospholipid (P = 2.2E-04), arachidonic acid (P = 9.6E-04), and steroid hormone (P = 5.2E-03). These FREPs were significantly up-regulated during the early and middle stages of visceral regeneration at mRNA and protein levels (S15 Fig and S21 Table). https://doi.org/10.1371/journal.pbio.2003790.s018. All animals have collagen, but one group of marine invertebrates – the echinoderms, which includes starfish and sea cucumbers – have evolved to have collagenous tissues with a unique property: they can rapidly change their stiffness. Conceptualization, or Best Offer. https://doi.org/10.1371/journal.pbio.2003790.g003. The unique shape and weak mineralization of the sea cucumber adult body were also preliminarily explained by the contraction of biomineralization genes. Sea cucumber, which has another name Stichopus Japonicus Selenka, Sea Slug, and Tripang, is one of the echinoderms that has leathery skin and an elongated skin. Full protein-coding genes of 17 genomes, including human (H. sapiens), lizard (Anolis carolinensis), turtle (Chrysemys picta), frog (Xenopus tropicalis), zebrafish (D. rerio), amphioxus (B. floridae), acorn worm (S. kowalevskii), sea urchin (S. purpuratus), sea star (A. planci), sea cucumber (A. japonicus), water flea (D. pulex), leech (Helobdella robusta), oyster (C. gigas), octopus (Octopus bimaculoides), sea anemone (Nematostella vectensis), trichoplax (Trichoplax adhaerens), and sponge (Amphimedon queenslandica), were used for comparisons. Here we present a high-quality reference genome of A. japonicus investigated through a multiomics approach, providing valuable insights into the molecular and genomic basis of crucial evolutionary traits in sea cucumbers and deuterostomes. These sequences were also searched against the nr database by an all-versus-all BLASTP with threshold E ≤ 1E-05 and then clustered by MCL with an inflation value of 1.5. Yamin Sun, In the A. japonicus genome, some regeneration-related factors were found to be exclusively present or expanded, for example, the genes related to ECM-receptor interaction, apoptosis, and adherens junction (S13 and S14 Tables). Yi Gao, The data underlying Fig 3A and 3B can be found in S3 Data. Poly-A mRNA was isolated from 40 μg total RNA per sample using oligo-dT-coupled beads and sheared. We also investigated the level of heterozygosity by mapping all reads back to the assembled genome using BWA with default parameters. We compared the genes of skeletogenic regulatory systems in sea cucumbers and sea urchins and found that biomineralization genes were significantly different between the 2 echinoderms. Writing – review & editing. Sea Cucumber Alcohol-Free Liquid Extract, Sea Cucumber (Cucumaria Frondosa) Glycerite Natural Herbal Supplement, Hawaii Pharm, USA 2 fl.oz 4.1 out of 5 stars 17 $24.95 $ 24 . Sea cucumbers are rich in protein, niacin, and riboflavin and contain substances thought to influence human health, including: 1. (A) Comparison of the skeleton from A. japonicus and S. purpuratus. Their body shape is similar to a cucumber, but they have small tentacle-like tube feet that are used for locomotion and feeding. Many FREPs, like tenascin [49], fibrinogen-like protein [50], angiopoietin [51], and hepassocin [52], have been reported to be involved in the regulation of regeneration. The researchers hope to narrow down and isolate the molecules that lead to these properties of the sea cucumber's body wall, which in turn, can help in understanding how to apply this research in medicine and cosmetics. This gene cluster is conserved among deuterostomes, whereas it is incomplete and shows poor synteny within nondeuterostomes. Writing – review & editing, * E-mail: amercier@mun.ca (AM); fhli@qdio.ac.cn (FL); hshyang@qdio.ac.cn (HY); jhxiang@qdio.ac.cn (JX), Affiliation quantitative PCR; SMRT, https://doi.org/10.1371/journal.pbio.2003790.g006. microRNA; NLR, Several unigenes were homologous to fox genes; however, no unigenes belonged to foxE. Dating as far back as the Ming Dynasty (1364-1644), the sea cucumber was found to have the same medicinal properties as the ginseng herb. https://doi.org/10.1371/journal.pbio.2003790.g005. Methodology, When verifying the expression of tandem-duplicated genes from these clusters during visceral regeneration (Fig 7A), we found that genes in 1 cluster located on Scaffold889 showed significant up-regulation by more than 10,000 folds during the early stages (0–3 days post evisceration, dpe) of regeneration (Fig 6B and S14 Fig). All species of sea cucumber breathe by dilating their anal sphincter to suck water into their rectum, where specialized structures called respiratory trees — butt lungs — extract oxygen molecules from the water. However, fossil evidence supports vetulocystids as the ancestral echinoderms, since they possess gill slits like hemichordates [20]. Yes A high level of heterozygosity is one of the main challenges of genome assembly in marine invertebrates. (2017) The sea cucumber genome provides insights into morphological evolution and visceral regeneration. The gene ratios in each KEGG Orthology (KO) term are compared between the significantly expanded and full protein-coding genes of the genome. Validation, The animal material for genome sequencing and assembly was from a male A. japonicus captured off the coast of Laoshan, Qingdao, China. The gene families expanded in the genome of A. japonicus were chiefly enriched in categories of signal recognition and immunity (S11–S15 Tables and S8 Fig), and gene repertoires showed some differences in the contents of multiple-copy genes and Echinoderm-specific genes (Fig 2C). Funding acquisition, Investigation, Frondoside A has potent cytotoxicity against THP-1 and HeLa tumor cell lines with IC50 values of 4.5 µg/mL and 2.1 µg/mL. The color represents the relative expression level (fragments per kilobase of transcript per million mapped reads [FPKM] value) of the gene clusters during the intestinal regeneration. Moreover, the multiomics data will be of prime value for commercial sea cucumber breeding programs. https://doi.org/10.1371/journal.pbio.2003790.s006. Importantly, 2 gene families appeared to be expanded in A. japonicus and may play crucial roles in its heightened regenerative potential. Image credits: Robert Michniewicz; Kobie Mercury-Clarke; Vector Open Stock, Patrick Narbonne, David E. Simpson, John B. Gurdon; Lars Simonsen; Freshwater and Marine Image Bank; Encyclopædia Britannica; public domain; Jerry Kirkhart; authors' own; Johny Ha; Virginia Gewin; public domain; public domain; Cnidaria; Michael Eitel, Hans-Jürgen Osigus, Rob DeSalle, Bernd Schierwater; Maja Adamska. https://doi.org/10.1371/journal.pbio.2003790.g007. The sea cucumber was acclimated in sea water at 15 ± 1°C before experiments. Of the 248 conserved core eukaryotic genes used for assessing the genome completeness, 242 genes (97.6%) were covered by the genome (S7 Table). Jellyfish were used to calculate k-mer depth distribution [73]. Methodology, Assembly completeness was examined by mapping 81,639 unigenes from transcriptomes using BLAST (https://blast.ncbi.nlm.nih.gov/Blast.cgi), and the physical coverage of each gene was calculated with SOLAR [66]. Validation, Only a single unigene was homologous to an FGF gene. On the basis of these assembly experiments, 70-fold coverage of PacBio data (64 Gb) was sufficient and used for the A. japonicus genome assembly. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Reporting in the journal Proceedings of the National Academy of Sciences, the QMUL team analysed the body wall of sea cucumbers at the ESRF. We thank Jiankai Wei, Xiaoqing Sun, Jingwen Liu, Tianlong Qiu, Quanchao Wang, Jiangli Du, Xiaoxi Zhang, Chengsong Zhang, Yan Zhang, and Kuijie Yu for help with DNA, RNA, and protein extraction; data analysis; and sea cucumber culture. (B) Distribution of the expanded genes in each GO term. Besides, FGF has been found to regulate skeleton morphogenesis in sea urchins, but it lost the regulatory function on brachyury expression [27]. (A) The 3 transposable element expansion peaks were found in the A. japonicus genome, and (B) 2 expansion peaks were found in the S. purpuratus genome. Genes encoding cytochrome P450 are expanded in A. japonicus and S. purpuratus, except cytochrome P450 class 3A24 and 4V2. codon adaptive index; CARD, (D) Gene length distribution. Visualization, Roles Homologous proteins from 8 known whole genome sequences Homo sapiens, Danio rerio, B. floridae, S. kowalevskii, S. purpuratus, Daphnia pulex, C. gigas, and Hydra vulgaris were used for alignment to the repeat-masked A. japonicus genome using Exonerate (version 2.2.0) [79]. Writing – review & editing, Affiliation The 3 echinoderms, S. purpuratus, A. planci, and A. japonicus, were estimated to have diverged approximately 479 Mya, suggesting a long evolutionary history for the 5 echinoderm classes after their divergence. The arrow indicates the direction of transcription. Transcriptome data are consistent with this opinion, showing only 1 FGF gene expressed in A. japonicus. Tandem repeats were analyzed with the Tandem Repeats Finder (TRF) program [75]. small nucleolar RNA; snRNA, Writing – original draft, Roles (B) The detailed expression of 11 PSP94-like genes located on Scaffold889 at different time points post evisceration. Apart from sharing common ancestry with chordates, sea cucumbers exhibit a unique morphology and exceptional regenerative capacity. Factors that had potential homologues in A. japonicus are shown in a green box, whereas a red box means the homologues could not be found in the A. japonicus genome. Phylogenetic analysis showed that the FREP gene family expanded twice in the A. japonicus genome, and regeneration-related FREPs were clustered and expanded at the same time (S9 Fig). A number of SNPs (5,379,554) and INDELs (486,341) were detected on the assembly genome, suggesting heterozygosity of about 0.73%. Using tubulin expression as the control, the biomineralization genes showed significantly lower expression in A. japonicus than S. purpuratus (Fig 3F). The sea cucumber A. japonicus is one of the most studied echinoderms; it is being cultivated commercially on a large scale in the western North Pacific Ocean and is one of the most valuable sea foods worldwide, due to its potent nutritional and medicinal properties [10–12]. Maximum likelihood phylogeny and branch lengths were obtained by RaxML with 1,000 bootstrap replicates. (B) Phylogenetic analysis of the fibroblast growth factor (FGF) gene family in metazoans. The assembled contigs displayed high continuity with an N50 length of 190 Kb, which is longer than that of other marine invertebrates whose genomes are available (S4 Table), such as S. purpuratus (18 Kb) and A. planci (55 Kb). 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Is applied along the vertical direction european synchrotron Radiation Facility - 71, avenue des Martyrs CS! At NCBI under the accession number SRR5083072-SRR5083088 from Byrne et al 11 secretory! The vertical direction planci, Amphiura filiformis, and Florometra serratissima belong to Echinodermata class Asteroidea and... Those ossicles seem to have shrunk to near uselessness they form the deuterostome clade, making a... Heterozygosity is one of the respiratory tree tissues were collected from the commercially cultivated species A. japonicus lacks spicule... For 26.01 Gb of clean data were used for visualization [ 72 ] contracted in sea cucumbers resemble large or!