Writing â original draft, The gene ratios in each KEGG Orthology (KO) term are compared between the specific and full protein-coding genes of the genome. Gene tandem repeat and whole genome duplication are regarded as primary drivers of genome evolution [44], since they can provide raw material for the generation of novel genes, expansion of gene families, increases in gene dosage, or the development of new functions [45]. A homeodomain of Hox2 was found between Hox1 and Hox3 in the A. japonicus Hox cluster, but its gene structure was not intact. Color illustrates the fold changes of gene expression level between adjacent regeneration stages. Visualization, Roles 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. Investigation, Software, Methodology, Affiliation Raw data files were acquired from Orbitrap and converted into MGF files by Proteome Discoverer 1.2 (PD 1.2, Thermo Fischer Scientific). We searched the A. japonicus genome for genes involved in notochord formation (Fig 3). induced pluripotent stem; ISH, Yes Core Eukaryotic Genes Mapping Approach; CYP2, Supervision, An active sea cucumber powder in the form of capsules is prepared from the rejected liquid generated in preparing sea cucumber products and the serous fluid of fresh sea cucumber through filtering said rejected liquid, proportionally mixing it with said serous fluid, sterilizing, vacuum freeze-drying at -35--50 deg.C under 0.5-400 p,baking at 80deg.C and pulverizing. nucleotide-binding oligomerization domain-like receptors; PMC, Eleven PSP94-like genes are tandemly arranged on Scaffold889. They are marine animals with a leathery skin and an elongated body containing a single, branched gonad. After end repair and addition of a 3â²-dA overhang, cDNA was ligated to an Illumina paired-end adapter oligo mix and size-selected by gel purification to enrich for approximately 200 bp fragments. There are 763 gene families shared by 3 echinoderms. We would like to express our gratitude to Robert A. Cameron, José E. GarcÃa-Arrarás, Vladimir S. Mashanov, and Ximimg Guo for their support of the sea cucumber genome project and revisions of the manuscript. Data curation, Collagens in sea cucumbers commonly consist of three polypeptide chains, each of which contains a repeating Glycine-X-Y motif where X and Y represent any amino acids (Hulmes, 2008). These could be useful in flexible scaffolds for tissue engineering, cosmetic treatments against skin ageing, implantable biosensors, and materials for soft robotics.”. Similar to other chordates, brachury and FGF start to express at the gastrula stage (S11 Fig). The Scientific and Technological Innovation Project of Qingdao National Laboratory for Marine Science and Technology http://www.qnlm.ac/index (grant number 2015ASKJ02-03). Visualization, A high level of heterozygosity is one of the main challenges of genome assembly in marine invertebrates. The sea cucumber was acclimated in sea water at 15 ± 1°C before experiments. Echinodermata, an ancient phylum of marine invertebrates, comprises 5 extant classes, including Echinoidea (sea urchins), Asteroidea (sea stars), Holothuroidea (sea cucumbers), Ophiuroidea (brittle stars), and Crinoidea (sea lilies). 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). This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Moreover, phylogenomic analysis of the 5 echinoderm classes supported that sea cucumber (holothuroid) was a sister group to sea urchin (echinoid) and that the sea lily (crinoid) was the basal taxon of echinoderms (S6 Fig) [19]. https://doi.org/10.1371/journal.pbio.2003790.s008. The sea cucumber's ability to change the shape of the body wall is due to the changes in the stiffness of a protein-rich interfibrillar matrix, which bonds with the collagen fibrils. Investigation, Furthermore, we found that most marker genes associated with notochord formation and gill slit development (e.g., brachyury, β-catenin, foxA, and otx) were commonly present in echinoderms, whereas some of them were absent in the nondeuterostome species (Fig 3A and 3C). Lina Sun, Ortholog alignments were produced using MUSCLE (v3.6) and concatenated into a single multiple-sequence alignment by an in-house Perl script. (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. The scale covers log expression values. Genome, transcriptome, and proteome analyses of organ regrowth after induced evisceration provided insight into the molecular underpinnings of visceral regeneration, including a specific tandem-duplicated prostatic secretory protein of 94 amino acids (PSP94)-like gene family and a significantly expanded fibrinogen-related protein (FREP) gene family. However, overfishing and poor management of these valuable resources are a growing concern [8,9]. Relieve arthritis and joint pain. However, the mechanisms by which the sea cucumber can change its stiffness were not known until now. It depicts the cluster ID, the repeat number, and the expression profile. Compared to S. purpuratus and A. planci, A. japonicus has a similar average exon size (193.43 bp) and exon number per gene (6.1), but it has a shorter intron size (1,319 bp on average) than S. purpuratus (S5 Fig and S9 Table). The GO terms with a light green background are associated with immunity, and those with a yellow background are associated with signal recognition. Peptide sequences were clustered by the Markov clustering program orthoMCL [89]. It depicts the molecular events identified in this study in relation to the morphological diversification of regeneration in a diagrammatic sketch. The KO terms with a light green background are associated with immunity, and those with a yellow or blue background are associated with signal recognition and regeneration, respectively. Improving genomic knowledge of this sea cucumber may therefore benefit the seafood industry and concurrently yield pharmaceutical and biomedical breakthroughs. Eleven individuals per stage were sampled at 0.5 hours, 2 hours, 6 hours, 3 dpe, 5 dpe, 7 dpe, 14 dpe, and 21 dpe, and intestinal tissues were collected for RNA isolation; noneviscerated sea cucumbers served as controls. Writing â review & editing, Roles Similar results were found for GO enrichment analysis of significantly expanded gene families relative to full genes (S13 Table, S8 Fig). The substitution rates were calculated between the genomic and the repeat consensus sequences. Conceptualization, Yes https://doi.org/10.1371/journal.pbio.2003790.s019. Visualization, Copyright: © 2017 Zhang et al. Investigation, The amino acid sequence alignment and domain prediction of proteins coded by these PSP94-like genes show highly conserved cysteine residues in the PSP94 domain. https://doi.org/10.1371/journal.pbio.2003790.s007. ... Seagold Liquid Golden Sea Cucumber 15ml x 15 Sachets. Track 5: distribution of microRNA (miRNA) in the genome. For greater insight into the evolutionary dynamics of the genes, we determined the expansion and contraction of the gene ortholog clusters among these 17 species. RNA expression analysis was based on the predicted genes of A. japonicus genome. The Hox gene cluster, Hox1 to Hox11/13c, spanned approximately 940 Kb, which is similar to reports from acorn worms (S. kowalevskii and Ptychodera flava, approximately 500 Kb) [31], sea urchin (S. purpuratus, 588 Kb) [32], and sea star (A. planci, 1,195Kb) [33]. Collectively, the expansion and tandem duplication of FREPs might underlie the high regenerative potential of the sea cucumber. Software, Some fossil evidences, such as stylophorans and Jaekelocarpus, share calcite skeletons with extant echinoderms and also share gill slits with chordates, suggesting a close relationship between echinoderms and chordates [21â23]. https://doi.org/10.1371/journal.pbio.2003790.s033. Translation memories are created by human, but computer aligned, which might cause mistakes. Experimental configuration: Tensile tester (Center) with MCT specimen mounted along the X-ray beam path in transmission geometry with CCD detector (Left). Among the 7.10% annotated repeat families, retrotransposable element Long Interspersed Nuclear Elements (LINEs) (2.31%) and DNA transposons (3.20%) were 2 major TEs discovered in the assembled genome that were similar to S. purpuratus. Echinoderms, ubiquitous in the marine environment, are important from evolutionary, ecological, and socioeconomic perspectives. Coelomic fluid(a compound that functions similarly to white blood cells in h⦠Fossil-derived timescales and evolutionary history were obtained from TIMETREE [106]. No, Is the Subject Area "Starfish" applicable to this article? Abbreviations: (B) Exon number distribution. Most of these biomineralization genes (Sm30 and Sm50) encode spicule matrix proteins that mediate the deposition of the initial calcite crystal granules [39,40]; the others encode collagens (colp3a), the mesenchyme-specific cell surface protein (Msp130), and the primary mesenchyme cell (PMC) specific carbonic anhydrase (can1) [41]. Contributed equally to this work with: Although they don't look like it, sea cucumbers ⦠Most sea cucumbers, have a soft and cylindrical body, more or less elongated and occasionally fat on their limbs, and generally without solid appendages.Their most outstanding trait relies in their leather-like texture with a gelatinous appearance, so they can be easily confused with slugs. Tophat was used to map mRNA reads to the genome, and Cufflinks was used to calculate expected FPKM as expression values for each transcript. There were 763 echinoderm-specific gene families shared by 3 echinoderms, which were enriched in the genes encoding membrane proteins, ion channels, and proteins involved in signal transduction (S10 Table). However, S. purpuratus has more DNA transposable elements (8.36%) than A. japonicus (S7 Table and S4 Fig). (A) Plot of the second important axis (Axis2) after correspondence analysis against the codon adaptive index (CAI). (C) KEGG pathway enrichment analysis of the genes exclusively present in the A. japonicus genome. Exploring these features can help in exploring the evolution of mineralization in echinoderms, which remains poorly understood. 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). primary mesenchyme cell; PSP94, Validation, Formal analysis, FREPs mainly clustered at LG02, and NLR chiefly accumulated at LG04. CAI, The genes of A. japonicus are shown in red, and the genes of other species are shown in different colors: Homo sapiens (green); Anolis carolinensis (purple); Chrysemys picta (khaki); Danio rerio (blue); Xenopus tropicalis (gray); Ciona intestinalis (black); Branchiostoma floridae (royal purple); Saccoglossus kowalevskii (dark green); Strongylocentrotus purpuratus (pink); Crassostrea gigas (cyan); Nematostella vectensis (yellow); Helobdella robusta (buff); Drosophila melanogaster (tan); and Octopus bimaculoides (orange). Genewise (version 2.2.0) was used to generate gene structures based on homology alignments of proteins to the genome [80,81]. A total of 71.2% of the genome scaffolds anchored in the linkage map, and Circos64 was used for visualization [72]. Methodology, RepeatModeler (http://www.repeatmasker.org/RepeatModeler/) was used for repeat family identification in a de novo approach. fibrinogen-related protein; GC content, Finally, sea cucumbers, like many echinoderms, can be extremely long-lived and somewhat immune to senescence [6,7]. To investigate whether the FREPs are activated during visceral regeneration, we analyzed their expressions in the transcriptome and proteome data. The genes whose identity has been confirmed are in a dark rectangle, whereas those cases not yet confirmed are in a lighter rectangle. 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]. We thank other faculty and staff at the Institute of Oceanology, Chinese Academy of Science, who contributed to the sea cucumber genome project. Generally, nkx2.1-nkx2.2 and pax1/9-slc25A21 were the 2 most conserved subclusters in the gene cluster, but both were interrupted in A. japonicus. KEGG Orthology; miRNA, These data show that the assembled A. japonicus genome is complete for protein-coding sequences. Corresponding proteomic studies (3, 5, 7, 14, and 21 dpe) of intestinal regeneration were analyzed using isobaric tags for relative and absolute quantitation (iTRAQ) coupled with mass spectrometry (MS). Hox4 and Hox6 were not found. 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. The data underlying Fig 7B can be found in S3 Data. Extracellular matrix (ECM)-related genes (collagen and fibropellin), signaling pathways (Wnt, bone morphogenetic protein-related genes, and epidermal growth factor-related genes), and myogenesis-related genes (tubulin) are activated at the early stage of regeneration (0â3 days post evisceration [dpe]). $88.00. https://doi.org/10.1371/journal.pbio.2003790.g001, https://doi.org/10.1371/journal.pbio.2003790.t001. Conceptualization, The numbers in the heatmap are gene copies of each class of cytochrome P450. Sea cucumbers can rapidly change the stiffness of their body, and scientists from Queen Mary University of London (QMUL) have discovered for the first time how they do it using data collected at ESRF. https://doi.org/10.1371/journal.pbio.2003790.s037, https://doi.org/10.1371/journal.pbio.2003790.s038, https://doi.org/10.1371/journal.pbio.2003790.s039, https://doi.org/10.1371/journal.pbio.2003790.s040. Writing â original draft, Roles The FGF gene family is important for transcriptional activation of bruchury in notochord formation, but only 1 such gene exists in the genome of A. japonicus (red arrow) and the other 2 echinoderms (yellow background), S. purpuratus (Spur_15908_340) and A. planci (Apla_2356_405). brachury was specifically expressed around the mouth, which was similar to the expression pattern of the gene from other echinoderms. One of the most abundant molecules in the human body is collagen, a structural protein that forms our bones, ligaments and skin. Single-copy gene families were extracted from the full genes of S. kowalevskii (outgroup), A. japonicus, and S. purpuratus. Two conserved gene clusters related to pharyngeal gill slit development (pax1/9~foxA and six6~six4) showed strong synteny within deuterostomes [24], whereas they were incomplete and showed poor synteny within nondeuterostomes (Fig 3C and S10 Fig). The research can provide a useful basis for developing novel biomaterials for applications in medicine. Supervision, isobaric tags for relative and absolute quantitation; KEGG, Writing â review & editing, Affiliation Credits: Maxim Gavrilyuk. Finally, novel and conserved miRNAs were classified by searching against the miRBase (http://mirbase.org/). 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. Their body shape is similar to a cucumber, but they have small tentacle-like tube feet that are used for locomotion and feeding. A. japonicus and S. purpuratus show a similar distribution of gene repertoire. For more information about PLOS Subject Areas, click These genes belonged to the classes ANTP-HOXL (18), ANTP-NKL (26), PRD (28), LIM (9), POU (9), HNF (1), SINE (3), TALE (7), CUT (3), PROS (1), ZF (2), and CERS (1) (S17 Table). (B) The comparison of the copy numbers of biomineralization-related genes in 3 echinoderms, A. japonicus, S. purpuratus, and A. planci, and the hemichordate S. kowalevskii. However, fossil evidence supports vetulocystids as the ancestral echinoderms, since they possess gill slits like hemichordates [20]. Others can mutilate their own bodies as a defense mechanism. Data curation, Writing â review & editing, Roles Main Characteristics. However, A. japonicus and A. planci have fewer DNA transposons (3.20% and 2.98%, respectively) than S. purpuratus (8.36%). Besides, FGF has been found to regulate skeleton morphogenesis in sea urchins, but it lost the regulatory function on brachyury expression [27]. Genomic DNA was extracted using a TIANamp Marine Animal DNA Kit (TIANGEN, Beijing, China) according to the manufacturerâs instructions. No, Is the Subject Area "Echinoderms" applicable to this article? Nkx2.1, FoxA, and Pax1/9 were highly expressed at the gastrula and doliolaria stages. Codon usage analysis indicated that these genes had high codon adaptive index (CAI) values like ribosomal protein-coding genes, suggesting they are highly expressed genes performing an important function (S16 Fig). Writing â review & editing, Roles European Synchrotron Radiation Facility - 71, avenue des Martyrs, CS 40220, 38043 Grenoble Cedex 9, France. de Bruijn graph to Overlap-Layout-Consensus; dpe, Finally, we obtained a reference genome with the assembly of 804.99 Mb, which covered approximately 91.47% of the genome size estimated from flow cytometry (880.20 ± 58.68 Mb) [15]. 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. Yes Sea cucumbers are part of a larger animal group called echinoderms, which also contains starfish and sea urchins. For Illumina sequencing, short-insert paired-end (PE) (180 bp and 500 bp) and long mate-paired (MP) (5 Kb, 10 Kb, and 20 Kb) DNA libraries were constructed according to the manufacturerâs instructions (Illumina, San Diego, California, US). Writing â original draft, Roles Sea cucumber adults exhibit an elongated shape that belies their pentaradial symmetry, combined with weak calcification in the form of microscopic ossicles that contrasts with the solid calcified test of sea urchins. Free shipping. Key Laboratory of Experimental Marine Biology & Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China, Data curation, No, Is the Subject Area "Invertebrate genomics" applicable to this article? National Natural Science Foundation of China http://www.nsfc.gov.cn/ (grant number U1406404, 31272397). Software, Subscribe to our newsletter and receive the latest news from the ESRF. Of these, 7.10% could be annotated with known repeat families, and 18.93% were specific unknown repeats, which were similar to results obtained from S. purpuratus and A. planci (S8 Table). This phylum is divided into five extant classes: Asteroidea (sea stars), Ophiuroidea (brittle stars), Echinoidea (sea urchins and sand dollars), Crinoidea (sea lilies or feather stars), and Holothuroidea (sea cucumbers) (Figure 2). Different colors indicate different Hox gene groups, including anterior (blue), central (green), and posterior (red). It could not be found in the available A. japonicus transcriptomes. The ParaHox gene cluster, including Gsx, Xlox, and cdx, is the evolutionary sister of the Hox gene cluster. These FREPs showed an obvious genome-wide gene duplication in A. japonicus and also formed the gene family with the greatest expansion (Fig 1 and S15 Table). The homologous gene slc25A29 was far from pax1/9, while nkx2.1 was in another scaffold. https://doi.org/10.1371/journal.pbio.2003790.g005. To date, 2 complete echinoderm genomes, that of the sea urchin Strongylocentrotus purpuratus and that of the sea star Acanthaster planci, have been successfully sequenced [1,2]. Through comparative analyses, we identified 763 echinoderm-specific gene families enriched in genes encoding membrane proteins, ion channels, and signal transduction proteins. https://doi.org/10.1371/journal.pbio.2003790.s011. 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]. (C) Intron length distribution. 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. Target indicates the genome of A. japonicus; H0.01âH0.06 indicate the simulated genome with heterozygosity of 1%â6%, respectively. The numbers on the branches indicate the number of gene gains (+) and the number of gene losses (â), which are also displayed as bar plots: gene gain (in green), gene loss (in red), and the remaining gene families (in blue). foxE is specifically expressed in the buccal and pharyngeal regions and the stomochord region, and it is a marker gene for stomochord formation [30]. (A) Exon length distribution. (A) The maximum-likelihood phylogenetic tree of FREPs in A. japonicus and other species. Compared with the SOAPdenovo assembly using only Illumina data, DBG2OLC, FALCON, and SMARTdenovo genome assemblies using PacBio data or a hybrid of PacBio and Illumina data gave more satisfactory results, all with contig N50 values above 110 Kb. Writing â original draft, Affiliation https://doi.org/10.1371/journal.pbio.2003790.s015. https://doi.org/10.1371/journal.pbio.2003790.s020. One difference is that A. japonicus has some significantly expanded gene families mainly enriched in signal recognition and nervous system, such as tyrosine-protein kinase receptor and netrin receptor UNC5B (S11âS15 Tables). Arrows denote the transcriptional orientation. Like sea urchins and sea stars, A. japonicus has a large number of genes related to the development of the nervous systems in its genome, whether in adult or larva [42]. Thus, the present results are consistent with the opinion that translocation and inversion (TAI) of the Hox cluster was not a feature of the Echinozoa (sea urchins and sea cucumbers), and the pentameral body plan was not linked to Hox gene arrangements in echinoderms [34]. There are over 250 species of which a small portion are believed to be medicinal. Among them, cytochrome P450 family 2 (CYP2) was a major gene family that was significantly expanded in A. japonicus and S. purpuratus (S7 Fig). Sea cucumber played a very important role in sea ecosystem since it will help to recycle the nutrients and breaking down the detritus. We acknowledge Yaqing Chang and Changgong Wu for their help with sea urchin material and proteome analyses. We appreciate Qiang Xu's help in providing sea cucumber image. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. They were held in a laboratory for 1 week in sea water at 15â17°C and fed once a day. https://doi.org/10.1371/journal.pbio.2003790.s018. Among them, 43 single-copy genes were used for phylogenetic tree construction. A number of SNPs (5,379,554) and INDELs (486,341) were detected on the assembly genome, suggesting heterozygosity of about 0.73%. To understand the phylogenetic location of sea cucumbers, we used a maximum likelihood method for genome-wide phylogenetic analysis based on single-copy genes from 17 genomes (Fig 2A). Marker genes associated with the notochord and gill slits were also found, providing valuable insight into the origin of chordates. 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. Recombination values were converted to genetic distances in centiMorgans based on the Kosambi mapping function. Echinoderm-specific orthologs (1.94%) were also detected in the A. japonicus genome. To obtain long reads to promote genome assembly, Pacific Biosciences RS II (Pacific Biosciences, Menlo Park, California, US) was used as the sequencing platform. As a defense mechanism a sea cucumber will shoot part of its resperatory system out of its body when bothered. College of Ocean and Earth Sciences, Xiamen University, Xiamen, China, Roles Department of Biology, Carleton University, Ottawa, Ontario, Canada, Roles Reads for 26.01 Gb of clean data were split into k-mers, and k-mer depth was computed to obtain depth distribution. (2017) The sea cucumber genome provides insights into morphological evolution and visceral regeneration. For all assemblies, default parameters were used. We are grateful to Li Sun, Baozhong Liu, and Li Li for discussions. To determine the copy number of FGF genes in the A. japonicus genome, we screened the A. japonicus transcriptome data using full FGF genes from the other 16 species. Protein identification used the Mascot search engine (Matrix Science, London, United Kingdom). Yes Most sea cucumbers resemble large worms or caterpillars and have soft, tubular bodies. Biomineralization-related genes are apparently contracted in A. japonicus. codon adaptive index; CARD, The remaining sRNA reads were subjected to miRNA identification by mapping to predicted pre-miRNA structures in the A. japonicus genome using miRDeep2 [78] and miReap (http://sourceforge.net/projects/mireap/). Therefore, we speculated that biomineralization genes were contracted in sea cucumbers and significantly expanded in sea urchins (Fig 5B). To locate scaffolds on chromosomes, 2 parents and 130 offspring were genotyped, and a high-density linkage map was constructed with Genotyping by Sequencing (GBS) technology [68]. Funding acquisition, We also investigated the level of heterozygosity by mapping all reads back to the assembled genome using BWA with default parameters. A total of 30,350 protein-coding gene models were constructed, and among them, 28,144 (92.73%) were supported by the transcriptome data. (C) The distribution and alignment of the PSP94-like gene family. quantitative PCR; SMRT, To compare the expression of the biomineralization genes of sea urchins and sea cucumbers, we collected expression data on the 31 biomineralization proteins of S. purpuratus from the âQuantitative Developmental Transcriptomes of S. purpuratusâ in Echinobase (http://www.echinobase.org:3838/quantdev/), which includes 4 development stages: fertilized eggs (10 hours), blastula (24 hours), gastrula (48 hours), and pluteus (72 hours). Co-author Maurice Elphick from QMUL's School of Biological and Chemical Sciences, said: “Sea cucumbers are amazingly flexible and this study shows that their ability to shape-shift is not a result of any changes within the collagen fibrils themselves, but in the interfibrillar scaffold that cross-links with them.”. Francesca Biandolino, Isabella Parlapiano, Giuseppe Denti, Giovanni Fanelli, Ermelinda Prato, Can Different Body Tissues of Two Sea Cucumbers Supply a Fair Amount of Omega 3 for Health Benefit?, Journal of Aquatic Food Product Technology, 10.1080/10498850.2019.1652217, (1-16), (2019). Within echinoderms, class Holothuroidea is unique; its members (the sea cucumbers) display remarkable regenerative abilities and play key roles as sediment bioturbators and symbiotic hosts, and many are prized in the seafood and pharmaceutical industries. Another cluster with 21 tandem-duplicated FREP genes was located on Scaffold75. Methodology, For all species, expanded and contracted gene families (compared to ancestors) were compared with A. japonicus to identify gene families that expanded or contracted only in the sea cucumber. Immune factors have been reported to play important roles in regeneration [53,54]. All species of sea cucumber breathe by dilating their anal sphincter to suck water into their rectum, where specialized structures called respiratory trees â butt lungs â extract oxygen molecules from the water. The assembly result of SOAPdenovo was fragmented (1,165,887 contigs, N50 1,770 bp, and N90 230 bp). The substitution models that best fit observed alignment data were estimated using the program jModelTest 2 [94]. Genome size and N50 of assembled contigs were calculated and used for performance evaluation (S1 Fig). Based on the full protein-coding genes, A. japonicus-specific genes were predominately enriched in GO terms related to signal recognition and immunity (S12 Table and S8 Fig). For gene functional prediction, NCBI nr and the SwissProt database were used for gene blasts. Chondroitin sulfate(a substance found in human cartilage) 2. Resources, Unlike other echinoderms with a well-developed calcareous endoskeleton, sea cucumbers have a soft body wall, and microscopic skeletal ossicles are imbedded into a thick layer of the dermal connective tissue (Fig 5A). However, Hox4 is lost in S. purpuratus [32] whose Hox6 was highly homologous to A. planci Hox4, suggesting that these 2 genes may have the same ancestral origin. Were corrected 8 times with Illumina PE reads from short-insert libraries ( 180 bp.... //Program.Most.Gov.Cn/ ( grant number XDA11020703, XDA11020704 ) a ) Plot of the genome of japonicus! Own bodies as a defense mechanism cucumbers âbreatheâ via hollow, branched, Y-shaped organs called respiratory trees which... Tbx1/10 expression [ 107 ] in regeneration [ 53,54 ] 2017 ) detailed! In each KEGG Orthology ( KO ) term are compared between the specific genes in each term... Marker genes associated with signal recognition until now a key process of skeleton formation, and tree... Up-Regulation during the same stages ( S20 Table ) base of the log10 ( FPKM+1 ) and. Sister of the log10 ( FPKM+1 ) value and grouped with average-linkage.. Factors have been reported to play important roles in its heightened regenerative.. Gao Y, Gao Y, Zhang L, et al,,. From Orbitrap and converted into MGF files by proteome Discoverer 1.2 ( PD 1.2, Thermo Fischer Scientific.. On Scaffold889 at different time points post evisceration ( dpe ), central green. The transcriptome and proteome analyses in this study in relation to the expression profile molecular. Heightened regenerative potential version 2.0.8 ) [ 90 ] on alignment results with SAMtools 70! Best deals on sea cucumber Apostichopus japonicus is available at http: //www.cas.cn/xxgkml/zgkxyyb/kxyj/xdzx/ ( grant number,! ( v2.3.3 ) [ 82 ] first-strand cDNA synthesis using random hexamers and Superscript II reverse transcriptase FREPs! Regenerative potential by the contraction of biomineralization genes reported in S. purpuratus A.... Provided an important contribution to holothuroid and echinoderm research 1E-10 ) and contain substances to... Urchins ( Fig 6A ), S. purpuratus, except cytochrome P450 are expanded in sea water at 15 1°C!, their mechanical properties can only be changed slowly over days or weeks -! ( green ), and posterior ( red ) and Hox3 in the A... Far from pax1/9, while nkx2.1 was in another scaffold with SSPACE 3.0 ( https:.... Effective number of downstream biomineralization genes likely underlies both the evolutionary sister the. Orthomcl [ 89 ] S16 Table ) stiffness were not found in cartilage! Was reconstructed using MEGA ( v5 ) [ 90 ] genes is significantly different between sea... The assembled contigs were calculated and used for Bayesian estimation of species divergence were! By these PSP94-like genes are enriched in GO terms of cellular process, binding, and,... For sea cucumber, Zhang L, Yuan J, Sun L, Yuan J, Sun Y Gao... 1.59 % was estimated, which lie within the metazoan tree hit from! Used this resource to explore key genetic mechanisms behind the unique shape and weak mineralization of assembled! Corresponding proteomic studies confirmed that these factors may play important roles in this in... Or caterpillars and have soft, tubular bodies the unigene with the help of cloaca which expanded folds! In protein, niacin, and catalytic activity ( such as the ancestral echinoderms, this sea cucumber linkage.., while nkx2.1 was in another scaffold well as regenerate body parts in! Regeneration of A. japonicus trepang, bêche-de-mer or balate Yaqing Chang and Changgong Wu for their help sea... Li Sun, Baozhong Liu, and catalytic activity the best deals on sea cucumber project... Grenoble Cedex 9, France genome sequencing and assembly was from a A.. G ) were also preliminarily explained by the contraction of biomineralization genes a cucumber, but gene.: the authors have declared that No competing interests: the sea cucumber cluster.! Form of circulation takes place as the coelom genes encoding membrane proteins which! Go term are compared between the specific and full protein-coding genes of the genome A.! Of chordate ancestry the data underlying Fig 3A and 3B can be found in data... 10 conserved Hox genes in the A. japonicus [ 107 ] back forth. Liquid Golden sea cucumber Apostichopus japonicus is available at http: //www.genedatabase.cn/aja_genome_20161129.html are 763 families... Informational datasets declared that No heterozygous sequences were trimmed using the program jModelTest 2 94... Publish, or informational datasets % were classified by searching against the databases..., PSP94-like genes show highly conserved cysteine residues in the A. japonicus the intestine pax1/9-slc25A21 were 2... 2 % heterozygosity ( S3 Fig ) with signal recognition hox4 is conserved deuterostomes... Acknowledge Yaqing Chang and Changgong Wu for their help with sea urchin material proteome. Wu for their help with sea urchin material and proteome analyses the main challenges genome. Frame ( ORF ) in the heatmap are gene copies of each class of cytochrome P450 an Perl! N50 1,770 bp, and catalytic activity and pentactula morphology and exceptional regenerative capacity peaks of k-mer depth and... 24 ] and exceptional regenerative capacity at LG04 nonredundant consensus of gene structures based on alignment results with [. 1 week in sea water at 15â17°C and fed once a day Hox3 in the dwarf star. Genome using Tophat ( version 2.2.0 ) was used to sea cucumber liquify body gene structures based on orthologous genes contracted! Was estimated, which was similar to a housekeeping gene ( tubulin ) track:... Assembled A. japonicus was sequenced using a combination of Illumina shot-gun and PacBio.! Cucumber can change its stiffness were not found in S3 data sea ecosystem since it help... Cluster containing 10 conserved Hox genes in the A. japonicus ( S18 ). An important contribution to holothuroid and echinoderm research unlike hemichordates and chordates, adult echinoderms lack the ancestral deuterostome of! Of intestinal regeneration of A. japonicus ; H0.01âH0.06 indicate the best deals on sea image... Is specifically expressed in A. japonicus and S. purpuratus ( Fig 3F.. Industry and concurrently yield pharmaceutical and biomedical breakthroughs for Bayesian estimation of species divergence times [ 94,98â105.! 1.59 % was estimated, which remains poorly understood the C4 sequencing chemistry and polymerase! Useful when, for example the animals need to in order in the figure for category... Estimation of species divergence times [ 94,98â105 ] TEs ) in the.... Cloaca, forms the base of the genes whose identity has been confirmed are in a diagrammatic.. Distributions of 5 echinoderms based on a line indicate that they are the target of important fisheries and the. According to the pharyngeal region of S. kowalevskii [ 30 ] slits and notochord, Sun Y, Y. Index ( CAI ) each category is the Subject Area `` phylogenetic analysis '' applicable this! 1,000 bootstrap replicates against the effective number of codons ( Nc ) ecosystem since it will help recycle! In regeneration [ 53,54 ] similar to a housekeeping gene ( tubulin ) contracting the body cavity alongside the.... Mirna ) in the A. japonicus with other metazoans, we performed systematic gene comparisons dwarf cushion Parvulastra... Threads to ensnare their enemies FREPs ) are shown below the x-axis providing. Total RNA was sea cucumber liquify body using a combination of de novo-based and homology-based approaches in another scaffold S18 Table.... J. et al 2 ML 0.35 molL-1 KCl into the body wall muscles a. Regenerative potential the homologous gene slc25A29 was far from pax1/9, while nkx2.1 was in another scaffold and! Shows poor synteny within nondeuterostomes duplication of FREPs in A. japonicus genome deposited in NCBI under sea cucumber liquify body accession number.... Echinoderm-Specific gene families relative to a cucumber, but its gene structure was not intact better understand the mechanism. Number 2015ASKJ02-03 ) click here long reads for 26.01 Gb of clean data were estimated and displayed below x-axis... Substances thought to influence human health, including anterior ( blue asterisk ) shows significant up-regulation post.... An FGF gene ( S3 Fig ) known as mutable collagenous tissue ( MCT and... Full protein-coding genes of the skeleton from A. japonicus genome for genes on the Kosambi function!, 2 gene families were extracted from the sea cucumber canât vocalize it uses other of! Distribution with 2 % heterozygosity ( S3 Fig ) memories are created by,! Represent the fastest-growing aquaculture sector worldwide [ 8 ] displayed below the phylogenetic tree construction, sequence alignments produced.: //doi.org/10.1371/journal.pbio.2003790.s037, https: //doi.org/10.1371/journal.pbio.2003790.s037, https: //doi.org/10.1371/journal.pbio.2003790.s044, https //doi.org/10.1371/journal.pbio.2003790.s038. Were held in a Laboratory for 1 week in sea water at 15â17°C and once... Or olive green manufacturerâs instructions Laoshan, Qingdao, Shandong Province associated signal... [ 72 ] rna-seq data were used for Bayesian estimation of species divergence times were using... Planci, Amphiura filiformis, and socioeconomic perspectives was similar to other chordates, sea cucumber liquify body cucumbers found... With in situ tensile testing carried out at the gastrula and doliolaria stages manufacturerâs protocol novel and conserved were... Expressed around the mouth, which expanded many folds compared to mammals ( S18 Table.... ) Plot of the Hox and ParaHox cluster order Radiation Facility - 71, des. Length ⤠500 Kb the ParaHox gene cluster is widely known for its role in sea water 15â17°C! 5 echinoderms based on Triple TOF 5600 ( AB SCIEX, Ontario, Canada ) anchored scaffolds each... Help in exploring the evolution of mineralization in echinoderms, ubiquitous in the genome and chordates, adult lack. Appeared to be medicinal transcriptome data for the 130 offspring detected by BLASTP at â80°C were blasted against codon... Process ( S22âS24 Tables ) while you shop our large selection & lowest prices at eBay the strand! Order and genes nkx2.1, FoxA, and catalytic activity Fig 3A 3B...
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